Chapter 12: The Vestibular System and Eye Movements

During takeoff in a jet you experience a particularly salient function of the vestibular system: sensing body acceleration. Although perception of signals from the vestibular sensory organs occurs only under special circumstances, this system is operating continuously by controlling relatively automatic functions, such as maintaining balance when we are walking on uneven terrain or adjusting blood pressure when we stand up quickly. The vestibular system shares many brain stem circuits and functions with the neural systems for controlling the extraocular muscles that move the eyes. Eye movement must be precisely controlled to position the image of an object of interest over the fovea, where visual acuity is best (see Chapter 7). The vestibular and oculomotor systems coordinate the head and eyes during head movement. Consider your ability to maintain gaze on a friend's face in a crowded airport terminal as you run toward her. Your head bobs up and down, and from side to side, but you can maintain fixation effortlessly. The vestibular system detects your head motion, and the oculomotor system makes compensatory eye movements to stabilize the image of your friend on the retina. The actions of the two systems are coordinated automatically by the vestibuloocular reflex. In addition, the medial descending motor pathways (see Chapter 10) assist in this action by adjusting head position by controlling neck muscles. This happens without conscious awareness, apart from knowing where to fixate your gaze.

From a clinical perspective, the vestibular and eye movement control systems are also very tightly linked. An important part of testing the integrated functions of the brain stem involves careful assessment of a person's ability to coordinate eye movement during head motion. Assessment of vestibuloocular reflexes is an important part of examination of the comatose patient. This chapter also continues the examination of the cranial nerve nuclei, through which greater knowledge of brain stem regional anatomy will emerge, and the descending motor pathways. Such knowledge is essential for clinical problem solving, for example, in understanding behavioral deficits and identifying the locus of central nervous system damage after a stroke. Because each of the cranial nerve nuclei has a clearly identifiable sensory or motor function, the clinician can thoroughly test the integrity of such functions.

Vestibular receptors sense head motion, both linear—such as that experienced during fast acceleration in an elevator or a jet—and angular—such as during turning. These receptors are located in five peripheral vestibular organs (Figure 12–2, inset): the three semicircular canals, which signal angular acceleration, and the utricle and saccule, which signal linear acceleration. Vestibular receptors are hair cells, which are innervated by bipolar neurons whose cell bodies are located in the vestibular ganglion. The axons of these bipolar neurons travel to the brain stem in the vestibular division of cranial nerve VIII and terminate in the vestibular nuclei. There are four separate vestibular nuclei: inferior, medial, lateral, and superior (Figure 12–2). The vestibular system comprises distinctive circuits that have the following major functions, each considered below: (1) perception, (2) blood pressure regulation, and (3) descending control of proximal and axial muscles. The vestibular system has a fourth major function in eye movement control; this is considered in the next section, on gaze control.

An Ascending Pathway From the Vestibular Nuclei to the Thalamus Is Important for Perception, Orientation, and Posture

Originating primarily from the superior, medial, and inferior vestibular nuclei, the thalamic path ascends bilaterally to several sites within and around the ventral posterior nucleus (Figure 12–3B). Three major sites within the parietal lobe and insular cortex receive vestibular information (Figure 12–3A). The vestibular cortex in the (1) retroinsular cortex and (2) posterior parietal lobe play roles in conscious awareness of vestibular sensory activation and in sensing body orientation and the orientation of the world around us. A separate region, (3) area 3a (part of the primary somatic sensory cortex) is thought to participate in sensing head position in conjunction with proprioceptive afferents in neck muscles (see Chapter 4). Each of these cortical regions is also involved in controlling proximal muscles and posture, not directly like the corticospinal tract, but rather through their descending connections with vestibulospinal tract neurons, an indirect corticovestibulospinal tract.

The Vestibular System Regulates Blood Pressure in Response to Changes in Body Posture and Gravity

Blood pressure regulation is an integrated response involving primarily heart rate and vascular smooth muscle control. When we sit up quickly, blood must now flow against gravity. Maintenance of adequate blood flow to the brain is accomplished by a pressor reflex response, in which there are compensatory increases in heart rate and vascular smooth muscle tone. These responses are mediated by the autonomic nervous system (see Chapter 15). When this response is inadequate, such as when a person is taking certain medications for reducing blood pressure or diuretics, orthostatic hypotension can result. Vestibular regulation of blood pressure is accomplished through connections with the brain stem visceral integrative centers—the solitary, vagal, and parabrachial nuclei—that, in turn, regulate autonomic nervous system function (Figure 12–3A; see Chapters 6 and 15).

The Vestibular Nuclei Have Functionally Distinct Descending Spinal Projections for Axial Muscle Control

For axial muscle control, the vestibular nuclei receive information primarily from the cerebellum and cerebral cortex. The vestibular nuclei have two functionally distinct descending projections for balance and coordinating head and eye movements: the lateral and medial vestibulospinal tracts. These two descending motor pathways form a major portion of the medial descending motor pathways. The lateral vestibulospinal tract, which begins at the lateral vestibular nucleus, descends ipsilaterally in the white matter to all spinal levels (Figure 12–3C). This pathway is crucial for controlling posture and balance, which involves neck, back, hip, and leg muscles. Recall from Chapter 10 that even though a particular tract may have a unilateral projection, the medial descending pathways collectively exert a bilateral influence on proximal and axial muscle control because they synapse on commissural neurons (see Figure 10-16A). The medial vestibulospinal tract, which starts primarily at the medial vestibular nucleus, descends bilaterally in the white matter but only to the cervical and upper thoracic spinal cord (Figure 12–3B). The medial vestibulospinal tract plays a role in controlling head position in relation to eye position.

The position and movement of the eyes are controlled voluntarily and by vestibular reflexes. There are five types of eye movements:

1. Vestibuloocular reflexes use information from the semicircular canals to compensate for head motion by automatically adjusting eye position to maintain the direction of gaze.

2. Saccades are rapid movements that shift the fovea to an object of interest.

3. Smooth pursuit movements are slow and are used for tracking a moving object.

4. Vergence movements (either convergent or divergent) ensure that the image of an object of interest falls on the same place on the retina of each eye.

5. Optokinetic reflexes use visual information to supplement the effects of the vestibuloocular reflex.

With the exception of vergence, all eye movements are conjugate: The eyes move in tandem at the same speed and in the same direction. Vergence movements are disconjugate; the eyes move in opposite directions.

Each eye is controlled by six muscles, which operate as three functional pairs, with antagonistic mechanical actions (Figure 12–4A). The lateral and medial rectus muscles move the eye horizontally, abducting (looking away from the nose) and adducting (looking toward the nose), respectively. The superior and inferior rectus muscles elevate and depress the eye, particularly when the eye is abducted. Finally, the superior and inferior oblique muscles depress and elevate the eye, especially when the eye is adducted. Other actions of the extraocular muscles are indicated in Figure 12–4B.

The Extraocular Motor Neurons Are Located in Three Cranial Nerve Motor Nuclei

The oculomotor nucleus contributes most of the axons of the oculomotor (III) nerve, which exits the rostral midbrain. The oculomotor nucleus (Figure 12–5) innervates four of the six extraocular muscles: medial rectus, inferior rectus, superior rectus, and inferior oblique (Figure 12–4). This nucleus also innervates the levator palpebrae superioris muscle, an eyelid elevator. (A contingent of autonomic nervous system axons travels in the oculomotor nerve to innervate smooth muscle; see Chapter 15.)

The other two extraocular motor nuclei are the trochlear and abducens nuclei (Figure 12–5). Motor neurons in the trochlear nucleus give rise to the fibers in the trochlear (IV) nerve, which innervate the superior oblique muscle (Figure 12–4). This cranial nerve is the only one that exits from the dorsal brain stem surface. The trochlear nerve is further distinguished because all of its axons decussate within the central nervous system. The abducens nucleus (Figure 12–5) contains the motor neurons that project their axons to the periphery through the abducens (VI) nerve. Abducens motor neurons innervate the lateral rectus muscle (Figure 12–4). Unlike spinal and other cranial nerve motor neurons, extraocular motor neurons are not controlled by the primary motor cortex.

The Vestibuloocular Reflex Maintains Direction of Gaze During Head Movement

Stable fixation can be maintained on an object during head movement because the vestibular system generates eye movement control signals that compensate for head movements. For example, horizontal rightward movement of the head generates leftward conjugate movement of the eyes (Figure 12–6A). This movement is produced by excitation of left lateral rectus motor neurons and right medial rectus motor neurons. The lateral and medial rectus motor neurons are directly activated by vestibular neurons (Figure 12–6B), demonstrating the importance of automatic control of eye movement by head movement. In addition, the medial rectus motor neurons are indirectly activated by the internuclear neurons in the left abducens nucleus (Figure 12–6B, thin line). Although not shown in Figure 12–6B, the circuit for vestibuloocular control also ensures that the mechanical action of the muscle that moves the eye, termed the agonist muscle, is not impeded by contraction of the antagonistic muscles (the muscles whose mechanical action is opposite that of the agonist muscle). This process occurs through inhibitory connections with the motor neurons of antagonistic muscles. For example, when the left lateral rectus motor neurons are excited, the left medial rectus motor neurons are inhibited.

Voluntary Eye Movements Are Controlled by Neurons in the Frontal Lobe and the Parietal-Temporal-Occipital Association Cortex

Saccades are triggered by neurons in the frontal eye field, a portion of cytoarchitectonic area 8 (see Figure 2–19). This cortical territory receives subcortical inputs from the basal ganglia and cerebellum, transmitted via thalamic neurons. The frontal eye field projects to the superior colliculus (Figure 12–7A). The axons of these frontal lobe projection neurons descend within the anterior limb and genu of the internal capsule to the brain stem. Superior colliculus neurons, in turn, project to distinct regions of the pontine and midbrain reticular formation that directly control saccades through their monosynaptic connections to extraocular motor neurons. The frontal eye fields also project directly to these two reticular formation zones. For controlling horizontal saccades, the frontal eye fields project to neurons in the paramedian pontine reticular formation (Figure 12–7A, B). These neurons process control signals and, in turn, project to the abducens nucleus. The abducens nucleus is more than a motor nucleus because, in addition to containing lateral rectus motor neurons, it also contains internuclear neurons (Figure 12–7B). Signals from the paramedian pontine reticular formation trigger horizontal saccades by directly exciting lateral rectus motor neurons in the abducens nucleus and, via the internuclear neurons, indirectly exciting medial rectus motor neurons in the oculomotor nucleus. For vertical saccades, the frontal eye fields project to the rostral interstitial nucleus of the medial longitudinal fasciculus in the midbrain reticular formation (Figure 12–7A). Neurons in this nucleus coordinate the muscles that produce vertical eye movements (Figure 12–5B). A portion of the posterior parietal cortex within area 7 participates in saccade generation through its role in visual attention: You must first attend to a stimulus before looking at it. This region projects through the posterior limb of the internal capsule to the superior colliculus.

Smooth pursuit movements have a remarkably different control circuit, one that involves higher-order cortical visual areas, for computing the speed of the moving target, and the cerebellum (Figure 12–8). The cortical control of smooth pursuit eye movements begins in the middle temporal (also termed V5) and middle superior temporal visual areas (see Figure 7–15). From the cortex, axons descend in the posterior limb of the internal capsule to engage a brain stem and cerebellar circuit comprising the pontine nuclei, the flocculus (a portion of the cerebellum; see Chapter 13), and the vestibular nuclei (Figure 12–8). All three extraocular nuclei receive input from the vestibular nuclei; the vestibular axons course in the medial longitudinal fasciculus (MLF). Axons in the MLF originating from the vestibular nuclei are also especially important in stabilizing eye position when the head is moved (see next section). While the frontal eye field is essential for saccade generation, it also participates in smooth pursuit movements.

Vestibular Sensory Organs Are Contained Within the Membranous Labyrinth

The membranous labyrinth is filled with endolymph, an extracellular fluid resembling intracellular fluid in its ionic constituents: a high potassium concentration and a low sodium concentration (see Chapter 8). Vestibular receptor cells are hair cells, like auditory receptors, located in specialized regions of the semicircular canals (termed ampullae) (Figure 12–9, inset) and the saccule and utricle (termed maculae). The hair cells of the semicircular canals are covered by a gelatinous mass (termed the cupula) into which the stereocilia embed. Angular head movement induces the endolymph within the canals to flow, displacing the gelatinous mass, which in turn deflects the hair cell stereocilia. The utricle and saccule also have a gelatinous covering over hair cells in their maculae. Calcium carbonate crystals, embedded in the gelatin, rest on the stereocilia. Linear acceleration causes the crystals to deform the gelatinous mass, thereby deflecting the stereocilia. The saccule and utricle are sometimes called the otolith organs because otolith is the term for the calcium carbonate crystals. The semicircular canals, utricle, and saccule each have a different orientation with respect to the head, thereby conferring selective sensitivity to head movement in different directions. Benign positional vertigo is a condition in which calcium carbonate crystals move freely within the semicircular canals. Changing head position causes the crystals to stimulate the hair cells aberrantly, thereby causing vertigo.

Vestibular hair cells are innervated by the peripheral processes of vestibular bipolar neurons, the cell bodies of which are located in the vestibular ganglion. The central processes of these bipolar neurons, which form the vestibular division of cranial nerve VIII, course along with the cochlear division and enter the brain stem at the lateral pontomedullary junction (see Figure AI–6). Some vestibular axons project directly to the cerebellum (see Chapter 13). In fact, the vestibular sensory neurons are the only primary sensory neurons that have this privileged access to the cerebellum because of the special role of the vestibular system in controlling eye, limb, and trunk movements.

The Vestibular Nuclei Have Functionally Diverse Projections

The vestibular nuclei (Figure 12–10) occupy the floor of the fourth ventricle in the dorsolateral medulla and pons (Figure 12–2). This region is termed the cerebellopontine angle. The posterior inferior cerebellar artery (PICA) supplies blood to the vestibular nuclei (see Chapter 4). Occlusion of this artery can produce vertigo, an illusion of movement—typically whirling—of the patient or his or her surroundings. The vestibular nuclei have extensive intrinsic interconnections with components of the nuclear complex on the same and opposite sides that are important in the basic processing of vestibular signals. The lateral vestibular nucleus (also termed Deiters' nucleus) gives rise to the lateral vestibulospinal tract, important in maintaining balance. The medial vestibular nucleus, with a lesser contribution from the superior and inferior vestibular nuclei, gives rise to the medial vestibulospinal tract, for head and neck control. The inferior, superior, and medial, but less so the lateral, vestibular nuclei also give rise to bilateral ascending projections to the thalamus. The vestibular nuclei also participate in the reflex stabilization of eye movements, the vestibuloocular reflex (Figure 12–6). Vestibular axons projecting to the extraocular motor nuclei travel in the MLF (Figures 12–10 and 12–11). Together with the cerebellum, the vestibular nuclei help to organize a blood pressor response to changes in gravity forces acting on the circulatory system.

The Extraocular Motor Nuclei Are Located Adjacent to the MLF in the Pons and Midbrain

The MLF is a myelinated pathway that runs close to the midline and beneath the fourth ventricle and cerebral aqueduct, throughout most of the brain stem. In the pons and medulla, it is closely associated with the extraocular motor nuclei: the abducens, trochlear, and oculomotor nuclei. The rostrocaudal course of the MLF can be seen on a parasagittal myelin-stained section close to the midline (Figure 12–11A2).

Lesion of the oculomotor nucleus produces a down and out eye position

The oculomotor nucleus (Figure 12–11B1) innervates the medial, inferior, and superior rectus muscles; the inferior oblique muscle; and the levator palpebrae superioris muscle, an eyelid elevator. The motor axons run in the oculomotor nerve, coursing through the red nucleus and basis pedunculi en route to exiting into the interpeduncular fossa (Figure 12–12B). Oculomotor nerve damage produces a "down and out" resting eye position ipsilaterally, resulting from the unopposed actions of the lateral rectus muscle (producing the outward position) and the superior oblique muscle (producing the downward position).

There are three other important eye movement control centers in the midbrain. The first is the superior colliculus, essential for controlling saccadic eye movements (Figure 12–11B1). Receiving inputs directly from cortical eye movement control centers in the parietal and frontal lobes (Figure 12–7A), neurons in the deep layers of the superior colliculus project to the paramedian pontine reticular formation in the pons (for controlling horizontal saccades) and to the interstitial nucleus of the MLF (Figures 12–11B1 and 12–12A), the second midbrain control center. This nucleus organizes vertical eye movements through its connections with the oculomotor and trochlear nuclei. The third integrative center is the interstitial nucleus of Cajal (see Figure AII–15). This nucleus helps to coordinate eye and head movements, especially vertical and torsional movements. This nucleus contains neurons that project axons to the spinal cord (termed the interstitiospinal tract), for axial muscle control, and to the contralateral interstitial nucleus of Cajal (via the posterior commissure), for coordinating eye and axial muscle control bilaterally.

Knowledge of regional midbrain anatomy is clinically important because damage of the ventral midbrain produces a complex set of neurological deficits that disrupt eye movement control, facial muscle function, and limb movements. Branches of the posterior cerebral artery supply the ventral midbrain, and when these branches become occluded, the oculomotor nucleus, the third nerve, and the basis pedunculi are affected. In addition to producing the "down and out" eye position because of third nerve involvement, this damage results in limb and lower facial muscle weakness on the contralateral side because of involvement of the corticospinal and corticobulbar tracts in the basis pedunculi. Limb tremor can also occur due to damage of the red nucleus (see Figure 10–11) and nearby axons that connect the red nucleus and the cerebellum.

The trochlear nucleus is located in the caudal midbrain

Trochlear motor neurons, found in the trochlear nucleus (Figure 12–11B2), innervate the superior oblique muscle contralateral to its origin. The nucleus is located in the caudal midbrain at the level of the inferior colliculus, nested within the MLF. Trochlear motor axons course caudally along the lateral margin of the cerebral aqueduct and fourth ventricle, in the periaqueductal gray matter. The axons decussate in the rostral pons (Figure 12–5A), dorsal to the cerebral aqueduct, and emerge from the dorsal brain stem surface (Figure 12–5B). Lesion of the trochlear nerve paralyzes the superior oblique muscle, resulting in slight outward rotation of the eye (or extortion) because of the unopposed action of the inferior oblique muscle. The eye elevates slightly because of the unopposed action of the superior rectus muscle. A patient with this lesion compensates by tilting his or her head away from the side of the paralyzed muscle.

The abducens nucleus is located in the pons

The abducens nucleus (Figure 12–11B4) contains the motor neurons that innervate the lateral rectus muscle. The nucleus is located just beneath the floor of the fourth ventricle and is partially encircled by facial motor axons on their way to the periphery (Figure 12–10A, inset). The abducens nerve fibers course toward the ventral brain stem surface and exit the pons at the pontomedullary junction, medial to the facial nerve. Lesion of the abducens nerve paralyzes the ipsilateral lateral rectus muscle and results in the inability to abduct that eye.

Parasympathetic Neurons in the Midbrain Regulate Pupil Size

The Edinger-Westphal nucleus mediates two reflexes: pupil constriction in response to light and pupil constriction together with lens accommodation in response to near focusing. The pupillary light reflex is the constriction of the pupil that occurs when light hits the retina. Visual input from the retina passes, via the brachium of superior colliculus, directly to the pretectal nuclei (Figure 12–12). The pretectal nuclei project bilaterally to the Edinger-Westphal nucleus, which contains parasympathetic preganglionic neurons; pretectal axons cross to the contralateral side in the posterior commissure. Axons from the Edinger-Westphal nucleus travel with the oculomotor fibers in their path to synapse in the ciliary ganglion in the periphery. From there, postganglionic neurons innervate the constrictor muscles of the iris. The bilateral projection of pretectal neurons to the parasympathetic preganglionic neurons in the Edinger-Westphal nucleus ensures that illumination of one eye causes constriction of the pupil on the ipsilateral side (direct response in the lighted eye) as well as on the contralateral side (consensual response). Pupillary reflexes are an important component of assessing brain stem function during clinical examination, including examination of the comatose patient.

Pupillary dilation is mediated either by inhibition of the circuit for pupillary constriction or by the separate control of the iris by the sympathetic component of the autonomic nervous system (see Chapter 15). The pupillary dialator fibers join the third nerve close to the eye. As a consequence of this organization, damage to exiting fibers of the third nerve, such as by occlusion of a branch of the posterior cerebral artery, will spare the dilator fibers. Such a lesion produces pupillary dilation because of the unopposed action of the pupillary dilator fibers of the sympathetic nervous system, which are spared by the lesion.

Parasympathetic preganglionic neurons in the Edinger-Westphal nucleus of the midbrain participate in a second visual reflex, the accommodation reflex, which is the increase in lens curvature that occurs during near vision. This reflex is usually part of the accommodation-convergence reaction, a complex response that prepares the eyes for near vision by increasing lens curvature, constricting the pupils, and coordinating convergence of the eyes. These responses involve the integrated actions of the visual areas of the occipital lobe, along with motor neurons in the oculomotor nucleus that innervate the extraocular muscles and parasympathetic preganglionic neurons. Central nervous system pathology can distinguish different components of the visual reflexes. For example, in neurosyphilis the accommodation reaction is preserved but the light reflex is impaired. Patients with this condition have a classic neurological sign, the Argyll Robertson pupils: Their pupils are small and unreactive to light but get smaller when the patients accommodate. Distinct portions of the midbrain are supplied by paramedian, short circumferential, and long circumferential branches of the posterior cerebral artery (see Figure 4–4B1).

The action of levator palpebrae superioris muscle, an eyelid elevator, is assisted by the tarsal muscle, a smooth muscle under sympathetic nervous system control. Conditions that impair the functions of the sympathetic nervous system (see Chapter 15) can produce a mild drooping of the eyelid (pseudoptosis) resulting from weakness of the tarsal muscle. True ptosis is produced by weakness of the levator palpebrae muscle, the principal eyelid elevator. This effect can result from third nerve lesions or neuromuscular diseases, such as myasthenia gravis, an autoimmune disease that attacks the neuromuscular junction.

Eye Movement Control Involves the Integrated Functions of Many Brain Stem Structures

As discussed earlier, horizontal eye movements are controlled by signals from the frontal eye fields and superior colliculus to the paramedian pontine reticular formation that coordinate the actions of the lateral and medial rectus muscles. These circuits are well understood, so much so that lesions at different sites explain deficit horizontal eye movement control in humans (Figure 12–13). A lesion of the abducens nerve produces paralysis of the ipsilateral lateral rectus muscle, thereby preventing ocular abduction on the same side (Figure 12–13, lesion 1). The unopposed action of the medial rectus muscle can sometimes cause the affected eye to be adducted at rest (not shown in the figure).

Deficits after an abducens nerve lesion differ from those after a lesion of the abducens nucleus (Figure 12–13, lesion 2). As with the nerve lesion, the ipsilateral eye cannot be abducted because of destruction of the lateral rectus motor neurons. Here, too, the resting position of the eye may be adducted because of the unopposed action of the medial rectus muscle. The nuclear lesion has a second effect: The patient cannot contract the contralateral medial rectus muscle on horizontal gaze in the same direction as the side of the lesion. Hence, the patient cannot gaze to the lesion side. This is called lateral gaze palsy, and it occurs because the lesion also destroys the internuclear neurons that coordinate the lateral and medial rectus muscles (Figure 12–7B).

A more rostral lesion of the MLF, which spares the lateral rectus motor neurons but damages the axons of the internuclear neurons, produces internuclear ophthalmoplegia (Figure 12–13, lesion 3; at level of the pons in Figure 12–11B3). This lesion is characterized, on lateral gaze away from the side of the MLF lesion, by the lack of (or reduced) ability to contract the ipsilateral medial rectus muscle and thereby adduct that eye.

For lesions at sites 2 and 3 (Figure 12–13), a clever way to verify that the affected medial rectus muscle is not paralyzed is to demonstrate that the patient can converge both eyes to view an object at close distance. This eye movement requires activation of both medial rectus muscles. The neural mechanisms that coordinate convergence involve the visual cortex and midbrain integrative centers, not the internuclear cells of the abducens nucleus.

The Ventral Posterior Nucleus of the Thalamus Transmits Vestibular Information to the Parietal and Insular Cortical Areas

The vestibular nuclei project bilaterally to the thalamus. This ascending projection originates primarily from the medial, inferior, and superior vestibular nuclei. Unlike the auditory and somatic sensory systems, there is no single tract through which the ascending vestibular projection travels. Some fibers travel in the MLF, some in the lateral lemniscus, and others scattered in the brain stem gray matter. The principal thalamic target of the ascending vestibular projection is the ventral posterior nucleus (Figures 12–2, 12–3B, and 12–14). Although this nucleus is familiar as a somatic sensory relay, it serves other functions. The rostral region of the nucleus, adjacent to the ventral lateral nucleus (for motor control; see Chapter 10), receives vestibular input and projects to area 3a of the somatic sensory cortex, to integrate proprioceptive vestibular information. More dorsal and posterior parts of the nucleus, and adjoining nuclei, also receive vestibular information but project to the posterior parietal lobe and the retroinsular cortex, a region near the posterior end of the lateral fissure (Figure 12–14). There does not seem to be a single "primary" vestibular cortex, like some of the other sensory modalities. Rather, the vestibular cortical areas are interconnected to form a network that integrates vestibular inputs with joint proprioceptive information such as posture, orientation, and perception (eg, acceleration, vertigo). Many of these areas have descending projections to the vestibular nuclei, which, in turn, project to the spinal cord for controlling axial and proximal muscles. The organization of this system—corticovestibulospinal—is similar to the indirect corticospinal pathways from the frontal motor areas (see Figure 10–2).

Multiple Areas of the Cerebral Cortex Function in Eye Movement Control

Eye movements are not controlled by the primary motor cortex but rather by multiple regions in the frontal and parietal lobes. The frontal eye fields, corresponding to a portion of area 8, are the principal frontal lobe regions engaged in circuits for both saccadic and smooth pursuit movements (Figures 12–7 and 12–8). Two other frontal lobe areas contain neurons important for saccadic eye movements, the supplementary eye fields and the dorsolateral prefrontal cortex (Figure 12–14B). The frontal lobe eye movement control centers work together with neurons in the caudate nucleus (Figure 12–14A), a component of the basal ganglia (see Chapter 14). The parietal lobe site important for saccadic eye movements is located in area 7. This region receives visual information from the "where" pathway (see Figures 7–15 and 7–16). Two nearby areas, the middle temporal and middle superior temporal, which are also part of the where pathway, transmit visual information for guiding pursuit movements.

Vestibular System

Peripheral Vestibular Sensory Organs

There are five vestibular sensory organs: the three semicircular canals, the utricle, and the saccule (Figures 12–2 and 12–9). Receptor cells, located in specialized regions of the vestibular apparatus, are innervated by the distal processes of bipolar neurons located in the vestibular ganglion. The central processes of these bipolar neurons form the vestibular division of cranial nerve VIII (Figures 12–2 and 12–9). These fibers terminate in the vestibular nuclei, located beneath the floor of the fourth ventricle in the rostral medulla and caudal pons (Figure 12–2A).

Vestibular Nuclei and Their Projections

Four separate vestibular nuclei are located in the medulla and pons: the inferior vestibular nucleus, the medial vestibular nucleus, the lateral vestibular nucleus, and the superior vestibular nucleus (Figures 12–2A and 12–10). Neurons within the superior, lateral, and medial vestibular nuclei give rise to an ascending pathway to several sites within and around the ventral posterior nucleus of the thalamus (Figures 12–3 and 12–14). Three major sites within the parietal lobe and insular cortex receive and integrate this information (Figures 12–3A and 12–14): (1) area 3a, which is thought to participate in head position and neck motor control, and (2) the posterior parietal lobe and (3) the insular cortex, which play roles in the sensing of body orientation and the orientation of the visual world.

There are two vestibulospinal tracts (Figure 12–3B). The lateral vestibulospinal tract, which descends to all spinal levels, originates from neurons within the lateral vestibular nucleus (Figure 12–10). This pathway is important for balance and posture. The medial vestibulospinal tract, which originates primarily from neurons within the medial vestibular nucleus (Figure 12–10), descends only to the cervical spinal cord. This pathway is important in controlling head position for gaze. Vestibulospinal tract neurons terminate on motor neurons that innervate proximal limb and axial muscles as well as on interneurons that synapse on these motor neurons.

Eye Movement Control

Extraocular Muscles

Each eye is controlled by six muscles, which operate as three functional pairs, with antagonistic actions (Figure 12–4). The lateral and medial rectus muscles move the eye horizontally, abducting (looking away from the nose) and adducting (looking toward the nose), respectively. The superior and inferior rectus muscles elevate and depress the eyes, respectively, but particularly when the eye is abducted. Finally, the superior and inferior oblique muscles depress and elevate the eye, especially when the eye is adducted.

Extraocular Motor Nuclei

The oculomotor nucleus innervates the medial, inferior, and superior rectus muscles; the inferior oblique muscle; and the levator palpebrae superioris muscle. The motor axons course in the oculomotor nerve (Figures 12–5, 12–11, and 12–12). Motor neurons in the trochlear nucleus give rise to the fibers in the trochlear (IV) nerve, which innervate the superior oblique muscle (see Figures 12–4, 12–10, and 12–11). This is the only cranial nerve that contains decussated axons and exits from the dorsal brain stem surface (Figure 12–5).

The abducens nucleus contains the motor neurons that project their axons to the periphery through the abducens (VI) nerve and innervate the lateral rectus muscle (Figures 12–4 and 12–9).

Brain Stem Centers and Cortical Areas for Eye Movement Control

Saccadic eye movements are controlled by neurons in the frontal eye fields (Figure 12–6A) that project to the superior colliculus (Figures 12–7B and 12–11B1) and to the pontine and midbrain reticular formation (Figure 12–7). The cortical axons descend in the anterior limb of the internal capsule. Neurons in the paramedian pontine reticular formation (Figures 12–7 and 12–10) coordinate horizontal saccades through their projections to lateral rectus motor neurons and internuclear neurons in the abducens nucleus (Figure 12–9), which project to medial rectus motor neurons in the oculomotor nucleus (Figures 12–6, 12–11, and 12–13B). Neurons in the interstitial nucleus of the MLF (Figures 12–11 and 12–13A) control vertical saccades. Smooth pursuit eye movements are also controlled by neurons in the frontal eye fields but through connections with the pontine nuclei, cerebellum, and vestibular nuclei (Figures 12–8 and 12–14).