Abnormalities in any of these systems may result in degradation of visual acuity, blurring of vision, oscillopsia, or possibly some degree of motion sickness.
The pursuit, OKN, and saccadic systems are controlled by different anatomical pathways that converge at the level of the brainstem, sharing the same supranuclear neurons (including the paramedian pontine reticular formation for horizontal movements and the rostral interstitial nucleus of the medial longitudinal fasciculus for vertical movements), which then innervate the ocular motor cranial nerve nuclei. Their separate origins allow selective disruption of these ocular motor functions by disease processes. Likewise, targeted clinical examination of these systems allows the clinician to identify the affected system and discern the responsible disease process.
Even persistent foveal fixation on a stationary target requires eye movement control, because it causes attenuation of neuronal responses in the retina (described earlier). The degradation of image quality that results is countered by microsaccadic refixation movements. These eye movements are continuous, very small amplitude (0.1°–0.2° of visual angle) “square-waves.” The term square waves derives from the appearance of eye movement tracings, in which eye movements of equal amplitude and speed to the left and right have a brief intersaccadic interval that produces tracings in the shape of square waves (see Chapter 9). The to-and-fro movements are small enough that the image is maintained within the field of the fovea but large enough to provide a constantly changing image to photoreceptors, which enhances perceptual quality. As is true for most saccadic movements, there is a slight pause (180–200 ms) between movements (ie, an intersaccadic interval).
Anatomy and Clinical Testing of the Functional Classes of Eye Movements
Clinical examination of the central eye movement system includes assessment of fixation, VOR, OKN, saccadic and pursuit eye movements, and convergence (see Table 7-1). Each of these movements is controlled by dedicated anatomical pathways, the collective goals of which are to permit accurate eye movements to desired targets and to maintain the position of both eyes on targets of interest. Methods of assessing each subsystem are described in the following sections. A thorough assessment of ocular motility also requires a search for nystagmus (see Chapter 9).
Ocular Stability
The most straightforward test of ocular stability involves observing the patient’s ability to fixate on a target when the head and body are held stationary. Fixation testing may also reveal spontaneous nystagmus, which is most frequently caused by an imbalance of vestibular input to the ocular motor nuclei. Abnormal eye movements that occur secondary to vestibular dysfunction can be suppressed by visual fixation (and will worsen in the absence of visual input [see Chapter 9]).
Vestibular Ocular Reflex
The VOR holds images stably on the retina during brief, high-frequency rotations of the head, as routinely occur during walking. VOR responses are driven by the semicircular canals (for angular movements) and the otoliths of the utricle and saccule (for linear acceleration). Neural activity
(excitatory and inhibitory) from these structures passes along the vestibular nerves to the vestibular nuclei in the medulla of the brainstem; from there, the activity projects to the ocular motoneurons (ie, the vestibular ocular reflex pathway; see Chapter 1). The vestibular nuclei are strongly interconnected with the cerebellum, especially the anterior vermis, nodulus, and flocculus. Each of the semicircular canals innervates 1 pair of yoked extraocular muscles, which move the 2 eyes in the same plane as the canal. Each semicircular canal monitors rotational movements in both directions within its plane; these movements are controlled by 2 populations of neurons that show mutually antagonistic activity, depending on the direction of movement. The VOR response attenuates fairly quickly, but a “velocity storage” mechanism provides the VOR with a longer period of influence during more prolonged head movements.
Evidence of VOR dysfunction can be readily elicited on examination. Spontaneous nystagmus is a hallmark of an uncompensated vestibular imbalance. This assessment can be enhanced by viewing the fundus with a direct ophthalmoscope while looking for repetitive shifts in the position of the optic nerve head. This test is first performed while the fellow eye is allowed to fixate on a target. Next, the effect of removing visual fixation (which is achieved by covering the fixating eye) is judged. An increase in nystagmus after removal of visual fixation, while the head and body are held in a stable position, suggests the presence of an uncompensated imbalance of the peripheral vestibular system. A drift of the optic disc to the patient’s right (caused by drifting of the eyes to the left) reveals deficient vestibular input from the left vestibular end organ or nerve (see Chapter 9).
Horizontal head shaking for 10–15 seconds may induce a transient nystagmus after the head is held stable if there is an asymmetry (in the velocity storage signals) of the vestibular inputs. It is important to prevent the patient from visually fixating during the test, as fixation will suppress vestibular responses. This can be achieved by having the patient close his or her eyes in a dark environment, by using high-plus lenses (+20 D) on a trial frame, or by placing Frenzel goggles in front of both eyes. After the head shaking is completed, the eye movements should be examined in the still-darkened room with a light held to the side of 1 eye. Head-shaking nystagmus can result from either peripheral or central vestibular lesions.
The VOR gain (ie, the ratio of the amplitude of eye rotation to the amplitude of head rotation) can be assessed clinically with the head thrust maneuver or through ophthalmoscopy, which is more sensitive but also more difficult to perform. The head thrust maneuver requires the clinician to briskly turn the patient’s head (small amplitude) while the patient visually fixates on a target with his or her normal correction. The VOR system is the primary system reacting to this type of brief head movement. Normally, if the head is accelerated 10°, the eyes will move exactly 10° in the opposite direction to maintain foveation of a stationary target. Any imbalance in the VOR gain results in the eyes being off target at the end of the head thrust, and a refixation saccade is required to recapture the target. A defective response is observed when the head is rotated toward the side of the lesion.
Bilateral vestibular loss or hypofunction is easily assessed by measuring visual acuity during head rotations (dynamic visual acuity). While the patient reads the Snellen chart with the proper optical correction, relatively small horizontal or vertical head rotations at approximately 2 Hz are performed. Bilateral subnormal VOR gain will produce a mismatch between the amplitude of the eye and head movements, which will cause the intended target to fall off the fovea, and the acuity will fall by several lines (typically 4 or more) in bilateral vestibular loss.
Optokinetic Nystagmus
The OKN system maintains steady alignment of images on the retina during sustained rotation of the head (or environment). After about 30 seconds, the rotation-induced VOR will attenuate. Thereafter, the OKN system provides a sustained output for eye position control that counters the effects of persistent rotations. Thus, the vestibular and OKN systems act synergistically to align the eyes properly during head rotations. Nonetheless, the pursuit system, which is driven by visual attention to a target, is more influential in maintaining proper alignment during sustained rotations than the OKN system (which may be more important for this task in animals without foveae). Pursuit movements also contribute to ocular stability during brief head rotations that primarily activate the VOR.
The initial response of the OKN system is a pursuit movement (described later in the chapter). Thereafter, a contraversive, corrective involuntary saccade is mediated by the same vestibular neurons that respond to vestibular stimulation, although, as stated earlier, that vestibular input wanes when the driving stimulus is head rotation. Thus, during prolonged visual movement across the retina (eg, as occurs when one is running continuously), the OKN reflex can maintain adequate visual fixation even after any vestibular influence from head movement has waned. The integrity of the vestibular neurons can, therefore, be studied without using vestibular stimuli.
The OKN system cannot be isolated for testing in the clinical setting, as to do so requires that the moving stimulus fill the complete visual environment and be associated with a brief period of optokinetic after-nystagmus (OKAN) once the movement ceases. The rotating drum of black and white stripes that clinicians use in the office, although quite practical, subtends only a portion of the visual field and, in reality, tests only the pursuit and saccade systems.
Saccadic System
The saccadic system rapidly shifts the fovea to targets of interest. Saccades are ballistic movements that generally cannot be altered once initiated. The speed of saccades correlates with the extent of eye movement—larger-amplitude saccades are faster than smaller-amplitude saccades, a relationship referred to as the main sequence. Saccadic velocity may exceed 500° per second, which allows the eyes to move from primary position to the farthest extent of the temporal visual field in only 0.2 second. Saccadic duration is generally less than 100 milliseconds.
Volitional saccades are controlled by several areas of the cerebral cortex, including premotor zones that project to the frontal eye fields (FEFs) (see Chapter 1, “Saccadic system”). Activation of these fields produces conjugate, contralateral saccades. The descending pathways from the FEFs primarily innervate the contralateral paramedian pontine reticular formation but also communicate with several intermediate structures, including the basal ganglia and superior colliculi, which also participate in eye movement control. Eventually, the outflow from the FEFs via this network reaches the ocular motoneurons (cranial nerves [CN] III, IV, VI), where the speed is encoded by the impulse frequency, or pulse, and the amplitude by the impulse duration, or step (Fig 7-1). The pulse derives from the initial signal generated from the FEFs, whereas the integration of horizontal eye movements to supply the required neural signal to control the eccentric positioning of the eyes (ie, the step) is performed by the medial vestibular nucleus and the accessory nucleus of CN XII (known commonly as the nucleus prepositus hypoglossi) in the medulla. The supranuclear brainstem center for control of conjugate vertical and torsional eye movements is the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF), which is located in the midbrain. The integration of vertical eye movements to supply the step function that controls the eccentric positioning of the eyes is performed at the nearby interstitial nucleus of Cajal (INC). (Note that this structure is the homologue to the
accessory nucleus of CN XII, which performs the integrative function for control of horizontal eye movements.) Saccades and gaze holding are also strongly influenced by the cerebellum.
Figure 7-1 Generation of a saccadic eye movement. Omnipause (P) cells cease their discharge just before the onset of a saccade, allowing burst (B) cells to create the pulse that initiates the saccade. The pulse is received by the neural integrator (NI), which determines the appropriate step (dt) needed to maintain the eccentric position of the eyes and modulates the signal to the ocular motoneuron (OMN). The lower right trace (E) depicts the shift in eye position from baseline to a sustained eccentric position. Vertical lines represent individual discharges of neurons. Underneath each schematized neural (spike) discharge is a plot of discharge rate versus time. (Reproduced with permission from Leigh RJ, Zee
DS. The Neurology of Eye Movements. 3rd ed. Contemporary Neurology Series. New York: Oxford University Press; 1999.)
Saccades can be tested by having the patient rapidly shift gaze between 2 targets, such as the extended index fingers of the clinician’s outstretched hands, which are held to the left and right of the patient. The latency (duration from stimulus to movement), accuracy (arrival of the eyes on target), velocity, and conjugacy (degree to which the 2 eyes move together) of the movements should be monitored. A hypometric saccade is one that falls short of the intended target; 1–2 small catch-up saccades may be within normal limits. A hypermetric saccade is one that overshoots the target and is