Ординатура / Офтальмология / Английские материалы / The Neurology of Eye Movements_Leigh, Zee_2006

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STABILIZATION OF THE HEAD VOLUNTARY CONTROL OF EYE-HEAD

MOVEMENTS

Rapid Gaze Shifts Achieved by Combined Eye-Head Movements

Smooth Tracking with Head and Eyes EXAMINATION OF EYE-HEAD

MOVEMENTS

LABORATORY EVALUATION OF EYEHEAD MOVEMENTS

DISORDERS OF EYE-HEAD MOVEMENT Disorders of Head and GazeStabilization Disorders of Voluntary Head and Gaze

Control

SUMMARY

between the ocular motor and cephalomotor control systems. Rotations of the head are usually described as having components in one or more of three planes: horizontal (yaw, rotation about the Z or vertical axis), sagittal (pitch, rotation about the Y or interaural axis), and torsional or frontal (roll, rotation about the X or nasaloccipital axis). Likewise, displacements or translations of the head are described as having components along one or more of three axes: bob (vertical), surge (anteriorposterior), and heave (lateral).

When most animals visually track or acquire targets, they use a combination of eye and head movements. Likewise, in response to perturbations of the body, both eye and head movements are used to reflexively stabilize the line of sight. This behavioral cooperation is reflected in the anatomic and physiologic similarities between the head (cephalomotor) and the eye (ocular motor) control systems. With the evolution of a fovea and a large ocular motor range, however, it became advantageous to be able to move the eyes with the head still. Therefore, primates in general and humans in particular have evolved a high degree of independent control of the head and eyes. Even so, we frequently move our eyes and head together,503 and an analysis of the effects of disease on eye movements must consider the interactions

STABILIZATION OF THE HEAD

Head perturbations that occur during locomotion are a major threat to clear vision. Although the vestibulo-ocular reflex (VOR) can compensate for head rotations by producing compensatory eye rotations, its ability to do so is limited; for example, when head velocities exceed approximately 350°/sec, saturation is reached and the reflex no longer works adequately.130 Stabilization of the head in space reduces demands made of the VOR. How well is the head stabilized during locomotion? Measurement of the rotational perturbations of the head during walking or running in place indicates that angular head

velocity usually does not exceed 1007sec, even during running (Fig. 7-1A).44.71'72'95'128

The predominant frequencies of head perturbations principally lie in the range 0.5-5.0 Hz (Fig. 7-1B), although some harmonic frequencies may be as high as 20

Hz. The predominant frequency of vertical head perturbations (i.e., pitch rotations) is usually twice that of horizontal perturbations (i.e., yaw rotations).71 The reason for this is that the head is perturbed vertically (up and down) with each heel strike, but rotates horizontally (right

and left) with each successive pair of steps. During locomotion, the angle of head orientation in the sagittal plane with respect to gravity is held quite constant (standard deviation of 3°).128 It has been hypothesized that this head orientation is necessary to optimize the sensitivity of the

otolithic organs of the labyrinth, which sense linear accelerations. During running, the head may bob as much as 6 cm, and this becomes important if subjects view near targets.35'72 Normal subjects show a synchronization of head translations and rotations, so that when the head bobs up, it pitches down, and as it heaves laterally, it rotates medially.35'128

What mechanisms operate to hold the head as a relatively stable platform during locomotion? Four main factors have been studied in humans: (1) mechanical forces due to the inertial mass of the head and the muscles and tissues that support it;

(2) the vestibulocollic reflex (VCR),20'118 by which vestibular inputs activate neck muscles to stabilize the head with respect to space; (3) the cervicocollic reflex (CCR), the stretch reflex of the neck muscles,

which acts to stabilize the position with respect to the trunk;85-123 and (4) voluntary

control of the neck muscles.

For most head rotations occurring during natural activities, the inertial mass of the head and passive viscoelastic properties of the neck play a major role in maintaining stability.67'73 Although the mass of the head tends to make it resistant to perturbations, its eccentric carriage on the series of joints that form the neck pre-

disposes it to oscillations, especially in pitch.62'67-123'172 During pitch motion of

the head, caused by linear body motion, head stability is determined by both passive viscoelastic properties and active tone in the neck muscles.68

The contributions of the VCR and CCR are difficult to assess experimentally in normal human subjects, but they appear to play more of a role when the subject views or imagines an earth-fixed tar- get.73-92'93 Based on measurements of head stability and neck muscle electromyography, these reflexes may be more active

perturbations, the VCR and CCR work together to stabilize the head in space. However, during body perturbations, the CCR detracts from the ability of the VCR to hold the head steady in space. An alternative explanation is that the purpose of

Eye-Head Movements 265

these reflexes is to prevent oscillations of the head.123 Head perturbations induced by sudden, passive body rotations in patients who have lost one vestibular labyrinth cause increased head oscillations when they are rotated towards the lesioned side.124 To stop the head from oscillating, the VCR and CCR may adjust the ratio of viscosity to elasticity of the neck muscles and connective tissues.67'92

VOLUNTARY CONTROL OF EYE-HEAD MOVEMENTS

During natural activities, we commonly use a combined eye-head saccade to shift gaze towards a novel visual target or scan the environment.98 However, head movements occur during a variety of behaviors besides gaze-shifts, such as during communication and eating. Thus, independent control of eye and head movements is to be expected. Just how independent eye and head movements are during voluntary gaze shifts is debated. In cats, they seem to be closely coupled,74 but care is required in extrapolating such findings to primates, who have a larger ocular motor range and may use eye-head movements independently for more complex behaviors. In discussing gaze shifts achieved by combined movements of eye and head, it is necessary to distinguish between eye position in the head (eye position) and eye position in space (the angle of gaze or, simply, gaze). During viewing of distant targets, gaze is the sum of eye position and head position. During viewing of a near target, a correction is necessary to account for the eyes not being at the center of rotation of the head (see Laboratory Evaluation of Eye-Head Movements, below).

Rapid Gaze Shifts Achieved by Combined Eye-Head Movements

Rapid gaze shifts that are achieved by combined, rapid eye-head movements (eye-head saccades or gaze saccades) serve two related, but separate functions: (1) they bring the image of an object, detected in the retinal periphery, to the fovea,

where it can be seen best; and (2) they reorient the head and eyes in space so that a new part of the visual scene can be viewed using ocular saccades.100 The second type of rapid gaze change is the only one made by afoveate animals,32 and it assumes particular importance in animals with a limited ocular motor range. Note also that quick phases of nystagmus, which occur during vestibular stimulation, do not bring a specific object to the fovea. The purpose of quick phases is to keep the eyes within the working ocular motor range (i.e., prevent the eyes reaching the mechanical limits of the orbits). During selfrotation, quick phases reorient the eyes towards the oncoming visual scene.

During natural activities, most ocular saccades occurring without head movements are < 15°,5 and eye-head movements are used to make larger gaze shifts. The tendency to make an eye-head saccade, rather than a purely ocular saccade, is partly determined by the ocular motor range, which in humans is about ±50°. If targets are presented outside this range, then an eye-head saccade is necessary to acquire it. However, if visual targets are presented within the current ocular motor range, the tendency to make an eye-head saccade is influenced by how eccentric the eye would be in the orbit at the end of the gaze shift.144 Some individuals (headmovers) are more prone to make eye-head saccades while others (non-movers) tend not to,53 but for any individual, the propensity to make a head movement is fairly constant,144 unless visual demands change.113 These idiosyncratic differences are generally preserved regardless of whether the target is visual or auditory, a finding that has suggested that the propensity to make a eye-head saccade is determined in a common reference framework for these two sensory modalities.54-61

EYE-HEAD SACCADES TO UNEXPECTED AND EXPECTED TARGET PRESENTATIONS

Examples of eye-head saccades are shown in Figure 7-2. When the movement is towards a target that unexpectedly appears

in the periphery, the saccadic eye movement usually starts 200 msec after the target appears and precedes the head

movement by about 20-50 msec (Fig. 7-2A).66-158'164 During eye-head saccades,

the velocity of the head increases with the amplitude of the head movement; this main sequence of head movements differs from the main sequence of eye saccades in that the former shows no saturation for larger movements and is more variable.8'145'154'175 Centrifugal head rotations may be faster than centripetal rotations.126 Like eye saccades, these movements have a ballistic, preprogramed nature15 that is capable of adaptive changes in response to increases in head inertia or visual demands.56 When eye-head saccades with horizontal and vertical components are made in response to diagonal target jumps, the trajectories of eye and head differ, suggesting independent control mechanisms.157 During such gaze shifts, ocular torsion stays near zero.157a If two visual targets are briefly presented in succession, the ocular response to this double-step stimulus is towards the second target

whereas the head moves towards the first.134

A different pattern of eye-head coordination appears when the subject can anticipate the time and location of the next visual stimulus.14 In this "predictive" mode of tracking, the head begins to move several hundred milliseconds before the saccade (Fig. 7-2B), and both begin before the stimulus moves. When self-paced and repetitive gaze shifts are required, eye and head components are more closely synchronized98 than in response to nonpredictable target jumps.126 During tracking of a visual stimulus moving predictably in an illusory trajectory, eye and head components are similar affected, tracking the illusion rather than actual target motion.180 When subjects use combined eyehead movements during manual tasks, the latency and velocity of the eye movement are influenced by both gaze shift and hand movements.143 Thus, the evidence for a common control signal governing eye and head components of eye-head saccades is only supported by behavior during repetitive, predictable tasks.

INTERACTION BETWEEN THE

SACCADIC COMMAND AND

VESTIBULO-OCULAR REFLEX

During rapid gaze shifts achieved by combined eye-head movements, the saccadic

command interacts with the mechanisms that act to hold gaze steady. In normal subjects, the VOR is of prime importance in holding gaze steady. The cervico-ocular reflex (COR), which depends on proprioceptive afferents from neck muscles to the

vestibular nucleus,50'94-151 makes little contribution to the stabilization of gaze in humans,7'11'89'137 unless vestibular function has been lost.23'29-90 Information from cervical afferents, however, may contribute to the sensation of head position.18

What is the nature of the interaction between the saccadic command and the VOR during eye-head saccades? Bizzi and colleagues14'115 initially proposed that during eye-head saccades of up to 40° amplitude, there is a linear summation of the saccadic command and the VOR. One prediction of this hypothesis is that the speed and accuracy of eye-head saccades would be independent of the head movement. This is not the case for large eyehead gaze shifts. In both humans and monkeys, during large eye-head saccades, gaze velocity and duration are clearly influenced by head velocity (Fig. 7-3);10° if the subject deliberately moves the head slower, gaze velocity is reduced. This is strong evidence against the linear summation hypothesis. Further, if the head is perturbed during large eye-head saccades,

the eye movements produced indicate that the VOR is partially disabled.75'100'122'149-155

For smaller eye-head saccades (i.e., within the ocular motor range), however, linear

addition of the saccadic command and the VOR probably does occur.75'122-153

Such gaze shifts might concern foveation of an object that has already been seen (i.e., is within the current ocular motor range), and thus represents a different class of eye movement than large eye-head saccades.

Although there is some independence

of eye and head contributions to large gaze shifts,126 and the VOR may be discon-

nected,1343 some mechanism appears to monitor head movements so that the accu-

racy of the eye-head saccade is guaran- teed.100-122'138'153 So, for example, if the

head is unexpectedly braked during an eye-head saccade, gaze still lands on the target. This finding has lead to the proposal that head velocity information, although disconnected from the conventional VOR, is still available to control the duration of the saccadic burst neurons via a vestibulosaccadic reflex,100 a notion that has received electrophysiological support.171 These findings have led to the formula-

Figure 7-3. Demonstration of how the duration of an eye-head saccade can be influenced by the speed of the head movement. The behavior of eye (E), head (H), and gaze (G), are shown during eye-head saccades between targets 205° apart. In B, the subject deliberately moved his head more slowly than in A. In A, the duration (vertical dashed lines) was 250 msec; in B, 380 msec. (From Laurutis VP,Robinson DA. The vestibulo-ocular reflex during human saccadic eye movements. J Physiol (Lond) 1986;373: 209-33, with permission.)

tion of several different models for eyehead saccades.39.75'100'122,126.153

Like ocular saccades, rapid gaze shifts achieved by a combined eye-head movement are also capable of adaptation. Thus, if subjects wear goggles with an aperture that restricts the effective ocular motor range to a few degrees, they adapt by making more use of head movements that are specific for the residual ocular motor range.36'113 Adaptive changes of eye-head saccades to new visual demands partly transfer to eye-only saccades, which sug-

gests that the substrate for adaptation lies upstream of the site where separate eye and head command are programed.125

NEURAL SUBSTRATE FOR RAPID EYE-HEAD GAZESHIFTS

Electromyographic studies during eyehead saccades demonstrate a burst of activity in the agonist muscles of both the eye and neck and inhibition in the corresponding antagonists.14 Although extraocular and neck muscles may be activated almost synchronously, the head has a higher moment of inertia and does not begin to move until about 20 to 50 msec after the eye.176 In trying to understand how eye and head movements are coordinated during eye-head saccades, a useful "bot- tom-up" approach is to compare structures projecting to ocular motoneurons with those projecting to motoneurons in the cervical spinal cord that control voluntary head movements.132 Such anatomical studies indicate that the major projections to the cervical cord are from the reticular formation, including the gigantocellular head-movement region (see next section), the paramedian pontine reticular formation (PPRF), the mesencephalic reticular formation adjacent to the interstitial nucleus of Cajal, and the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) (see Fig. 6-3, Chap. 6). In addition, vestibular and fastigial nuclei (see Display 6-13) project to these cervical areas, but the superior colliculus does not directly.132 Projections from motor cortex to cervical cord in humans have been studied by percutaneous scalp stimulation which evokes electromyographic responses in the contralateral sternocleidomastoid, trapezius and splenius capitis muscles at short (6-12 msec) latency.55 Below, we review possible contributions of each of these regions to the generation of eye-head saccades.

The Gigantocellular Head-Movement Region

Anatomical and electrophysiological studies in monkeys have defined neurons within the nucleus reticularis gigantocellularis (see Fig. 6-2, Chap. 6) to be impor-

Eye-Head Movements 269

tant for generating head movements during eye-head gaze shifts.33'34'132 This region lies in the rostral medulla, between the posterior aspect of the abducens nucleus rostrally and the rostral third of the hypoglossal nucleus caudally. It lies caudal and ventral to the physiologically defined PPRF. Electrical stimulation here evokes head movements at a latency of about 30 msec. These evoked movements are usually ipsilaterally directed horizontal (yaw) rotations; sometimes pitch or roll movements are evoked. Electrical stimulation in the gigantocellular head-movement region does not produce saccadic eye movements, although vestibular eye movements occur during evoked head movement and hold gaze steady. Neurotoxic damage to this area in cats abolishes spontaneous head movements.147

The gigantocellular head-movement region receives a major input from the posterior part of the superior colliculus, from the mesencephalic reticular formation surrounding the riMLF and interstitial nucleus of Cajal, from the medial pontine reticular formation, and from the fastigial and vestibular nuclei (see Fig. 6-3, Chap. 6). It projects to the upper cervical cord, via the anterolateral funiculus and the medial longitudinal fasciculus, to terminate in lateral parts of the ventral horn. Here axons contact cervical interneurons that also receive vestibulospinal inputs. These interneurons project to motoneurons that innervate rectus capitis, obliquus capitis, and splenius capitis muscles. It has been suggested that the gigantocellular headmovement region contributes to a variety of behaviors, such as feeding, as well as eye-head gaze shifts. Since electrical stimulation here does not produce gaze shifts, it appears that prenuclear inputs must synchronize movements of eyes and head. The frontal eye fields do not appear to project directly to the gigantocellular premotor area, and thus, inputs from the superior colliculus seem to be crucial for programing eye-head gaze saccades.

Role of the PPRF in

Eye-Head Saccades

Two classes of burst neurons in the PPRF of alert monkeys have been defined: those