Neural Control of Eye Movements

Introduction

Three fundamental visual sensory-motor tasks

The neural control of eye movements is organized to optimize performance of three general perceptual tasks. One task is to resolve the visual field while we move either by translation or rotation through space (self motion). Our body motion causes the image of the visual field to flow across the retina and reflexive eye movements reduce or stabilize this image motion to improve visual performance. The second task is to resolve objects whose position or motion is independent of the background field (object motion). Eye movements improve visual resolution of individual objects by maintaining alignment of the two foveas with both stationary and moving targets over a broad range of directions and distances of gaze. The third task is to explore space and shift attention from one target location to another. Rapid eye movements place corresponding images on the two foveas as we shift gaze between targets lying in different directions and distances of gaze.

Three components of eye rotation

All three perceptual tasks require three-dimensional control of eye position. These dimensions are controlled by separate neural systems. As described Chapter 8 , three pairs of extraocular muscles provide control of horizontal, vertical, and torsional position of each eye. Eye movements are described as rotations about three principal axes as illustrated in Figure 9.1 . Horizontal rotation occurs about the vertical Z-axis, vertical rotation about the horizontal X-axis, and torsion about the line of sight or Y-axis. As described in Chapter 8 , the amount of rotation about each of the three principal axes that is needed to describe a certain direction of gaze and torsional orientation of the eye depends upon the order of sequential rotations (e.g. horizontal, followed by vertical and then torsional). Some oculomotor tasks, such as retinal image stabilization, utilize all three degrees of freedom whereas other tasks, such as voluntary gaze shifts, only require two degrees of freedom, i.e. gaze direction and eccentricity from primary position. As described by Donder's law, torsional orientation of the eye is determined by horizontal and vertical components of eye position. Ocular torsion is independent of the path taken by the eye to reach a given eye position and is constrained by the gaze direction. Listing's law quantifies the amount of ocular torsion at any given eye position, relative to the torsion of the eye in primary position of gaze.

Figure 9.1, The three principal axes of eye rotation. Horizontal rotation occurs about the vertical axis (Z), vertical rotation about the transverse axis (X), and torsion about the anterior–posterior axis (Y).

Binocular constraints on eye position control

Binocular alignment of retinal images with corresponding retinal points places additional constraints on the oculomotor system. Because the two eyes view the world from slightly different vantage points, the retinal image locations of points subtended by near objects differ slightly in the two eyes. This disparity can be described with three degrees of freedom (horizontal, vertical, and torsional components) that are analogous to the angular rotations of the eye shown in Figure 9.1 . The main task of binocular eye alignment is to minimize horizontal, vertical, and cyclodisparities subtended by near targets on the two foveas. This requires a conjugate system that rotates the two eyes in the same direction and amount, and a disconjugate system that rotates the visual axes in opposite directions. As described by Hering, a common gaze direction for the two eyes is achieved by a combination of conjugate and disconjugate movements that are controlled by separate systems. The version system controls conjugate movements and the vergence system controls disconjugate movements.

Pure version and vergence movements are described respectively by the isovergence and isoversion contours shown in Figure 9.2 . The isovergence circle describes the locus of points that stimulate the same vergence angle in all directions of gaze. A different isovergence circle exists at each viewing distance. The isoversion lines describe the locus of points that stimulate the same version angle over a range of viewing distances in a common direction of gaze relative to the head. Pure vergence movements occur along any of the isoversion lines and not just along the central or midsagittal plane. Fixation changes along any other contour result from a combination of version and vergence movements. Both version and vergence movements are described as combinations of horizontal, vertical, and torsional rotations. For example there can be horizontal and vertical version and vergence movements. Torsional rotations are usually referred to as cyclorotations (e.g. cycloversion or cyclovergence). Hering's law implies that there is equal innervation of yoked muscle pairs: “one and the same impulse of will directs both eyes simultaneously as one can direct a pair of horses with single reins.” The law should not be taken literally, because common gaze commands from higher levels are eventually parceled into separate innervation sources in the brainstem that control individual muscles in the two eyes.

Figure 9.2, Geometric representation of the two components of eye movements by locations of the intersections of the two visual axes. The value in degrees marked along each isovergence circle denotes the convergence angle and the value in degrees marked on the hyperbola isoversion lines denotes the visual direction when a line is not very close to the eyes.

Feedback and feedforward control systems

The oculomotor system requires feedback to optimize sensory stimuli for vision with a sufficiently high degree of precision. Feedback provides information about motor response errors based upon their sensory consequences, such as unwanted retinal image motion or displacement. This visual error information usually arrives too late to affect the current movement, because the time delays in the visual system are about 50–100 msec. Instead, it is used to adaptively adjust motor responses to minimize subsequent errors. Oculomotor systems use sensory information to guide eye movements in two different ways. Motor responses can be guided in a closed-loop mode with an ongoing feedback signal that indicates the difference between the desired and actual motor response, or they can operate without concurrent feedback in an open-loop mode. The closed-loop feedback mode is used to reduce internal system errors or external perturbations. A physical example of a closed-loop system is the thermostatic regulation of room temperature, e.g. if the outside temperature drops, the furnace will turn on so that the room temperature stays constant. Motor responses can also be controlled in an open-loop mode, without a concurrent feedback signal. A physical example of an open-loop system is a water faucet, e.g. if the pressure drops, the flow of water will also drop, because the valve does not compensate for the pressure drop.

The mode of the response depends on the latency of the response, its duration and velocity. In most examples, visual feedback in a closed-loop system is used to maintain or regulate a fixed position or slow movements of the eyes when there is adequate time to process the error signal. Errors in eye posture or movement are sensed from displacement of the object of regard from the fovea or slippage of the retinal image and negative feedback control mechanisms attempt to reduce the errors to zero during the response.

Feed-forward control systems do not utilize concurrent visual feedback and are described as open-loop. These systems can respond to non-visual (extra-retinal) stimuli, or they respond to advanced visual information with short latencies and brief durations. For example, brief rapid head movements stimulate vestibular signals that evoke compensatory eye movements to stabilize the retinal image. These head movements can produce retinal image velocities of 300–400 deg/sec, yet the eyes respond with a counter rotation within 14 msec of the movement. The oculomotor response to head motion must rely on vestibular signals since retinal image velocities produced by head rotation exceed the upper velocity limit for sensing motion by the human eye. Retinal image velocities that exceed this upper limit appear as blurred streaks rather than as moving images. Visual feedback is not available when the response to head rotation begins because the latency is too short to utilize concurrent visual feedback. A minimum of 50 msec is needed to activate cortical areas that initiate ocular following, such that any motor response with a shorter latency must occur without concurrent visual feedback . Some open-loop systems, such as brief rapid gaze shifts (saccades), respond to visual information sensed prior to the movement rather than during the movement. Their response is too brief to be guided by negative visual feedback. Accuracy of a feedforward system is evaluated after the response is completed. Visually sensed post-task errors are used by feedforward systems to improve the accuracy of subsequent open-loop responses in an adaptive process that calibrates motor responses. Calibration minimizes motor errors in systems that do not use visual feedback during their response. All feed-forward oculomotor systems are calibrated by adaptation and this plasticity persists throughout life.

Hierarchy of oculomotor control

The following sections present a functional classification of eye position and movement control systems used to facilitate three general perceptual tasks and a hierarchial description of their neuro-anatomical organization ( Box 9.1 ). A hierarchy of neural control exists within each of the functional categories of eye movements that plans, coordinates, and executes motor activity. Three pairs of extraocular muscles that rotate each eye about its center of rotation are at the bottom of this hierarchy. The forces applied by these muscle pairs to the eye are controlled at the level above by the motor nuclei of cranial nerves III, IV, and VI. Motor neurons in these nuclei make up the final common pathway for all classes of eye movements. Axon projections from these neurons convey information to the extraocular muscles for executing both slow and fast eye movements. Above this level, premotor nuclei in the brainstem coordinate the combined actions of several muscles to execute horizontal, vertical, and torsional eye rotations. These gaze centers orchestrate the direction, amplitude, velocity, and duration of eye movements. Interneurons from the premotor nuclei all converge on motor nuclei in the final common pathway. Premotor neurons receive instructions from supranuclear regions including the superior colliculus, the substantia nigra, the cerebellum, frontal cortical regions including the frontal eye fields (FEF) and supplementary eye fields (SEF), and extrastriate regions including the medial temporal visual area (MT), the medial superior temporal visual area (MST), the lateral intraparietal area (LIP), and the posterior parietal area (PP). These higher centers plan the desired direction and distance of binocular gaze in 3-D space. Cortical–spatial maps of visual stimuli are transformed into temporal codes for motor commands between cerebral cortex and ocular motoneurons, to which the superior colliculus and cerebellum contribute. They determine when and how fast to move the eyes to fixate selected targets in a natural complex scene or to return them to a remembered gaze location. The following sections will discuss the hierarchical control for each of three functional classes of eye movements. The next section describes the final common pathway that conveys innervation for all classes of eye movements.

Box 9.1

Hierarchy of motor control

Subcortical oculomotor disorders are classified by lesion sites in the hierarchy of motor control:

Peripheral (cranial nerves and muscles)
Nuclear (cranial motor nuclei making up the final common pathway)
Premotor (coordinates combined actions of several muscles)
Internuclear (connections between nuclear and premotor sites)
Supranuclear (motor planning stage)

Final common pathway

Cranial nerves: III, IV, & VI and motor nuclei

Cranial nerves III, IV, and VI represent the final common pathway as defined by Sherrington, for all classes of eye movements. All axon projections from these cranial nuclei carry information for voluntary and reflex fast and slow categories of eye movements. The oculomotor (III), trochlear (IV), and abducens (VI) nuclei innervate the six extraocular muscles, iris and ciliary body. The abducens nucleus innervates the ipsilateral lateral rectus. Premotor interneurons also project from VI to the contralateral oculomotor nucleus for control of the contralateral medial rectus, to produce yoked movements on lateral gaze that are consistent with Hering's law. The trochlear nucleus innervates the contralateral superior oblique. The oculomotor nucleus innervates the ipsilateral medial rectus, inferior rectus, and inferior oblique, and the contralateral superior rectus. The anterior portion of the oculomotor nucleus also contains motor neurons that control pupil size and accommodation in a specialized region called the Edinger–Westphal nucleus. Afferents from this nucleus synapse in the ciliary ganglion prior to innervating their target muscles. The regions of the oculomotor nucleus that control various eye muscles are illustrated in Figure 9.3 .

Figure 9.3, Representation of motor neurons for right extraocular muscles in the oculomotor nucleus of monkey. Transverse sections at levels as indicated in the complex. DN, dorsal nucleus; VN ventral nucleus, CCN caudal central nucleus; IC, intermediate column, IV trochlear nucleus. Lateral and dorsal views are shown to the right.

Motor neuron response

The motor neurons control both the position and velocity of the eye. They receive inputs from burst and tonic cells in premotor nuclei. The tonic inputs are responsible for holding the eyes steady, and the more phasic or burst-like inputs are responsible for initiating all eye movements to overcome orbital viscosity and for controlling eye movements. All motor neurons have the following characteristics as illustrated in Figure 9.4 .

1
They have on–off directions (they increase their firing rate in the direction of agonist activity).
2
All cells participate in all classes of eye movements including steady fixation.
3
Each cell (especially tonic) has an eye position threshold at which it begins to fire. Motor neurons have thresholds that range from low to high. Cells with low thresholds begin firing when the eye is in the off field of the muscle that it innervates. Cells with higher thresholds can begin to fire after the eye has moved past the primary position by as much as 10 degrees into the on field of the muscle. The graded thresholds of motor neurons are responsible for the recruitment of active cells as the eyes move into the field of action for the muscle.
4
Increasing the frequency of spike potentials for a given neuron increases contractile force. Once their threshold is exceeded all cells increase their firing rate as the eye moves further along in the on direction of the muscle until they saturate. Cells increase their firing rate linearly as the eye moves into their on field.

Figure 9.4, Discharge rate of oculomotor neurons in relation to eye movement. On the left, the steady firing rate is shown when the eye is stationary; and below, the rate–position curve illustrates an increase of firing rate with eye position for four neurons. On the right, the firing rate is shown during a slow voluntary eye movement. The arrows indicate points where the eye passes through the same position with velocity of opposite signs, and the associated firing rate is different. Below, firing rate is plotted for a single unit and a particular deviation of the eye as a function of eye velocity. 11

Functional classification into three general categories

I

Stabilization of gaze relative to the external world

Movements of the head during locomotion tasks such as walking are described by a combination of angular rotations and linear translations. The oculomotor system keeps gaze fixed in space during these head movements by using extra-retinal and retinal velocity information about head motion. The primary extra-retinal signal comes from accelerometers in the vestibular apparatus.

A

Extra-retinal signals

The vestibular system contains two types of organs that transduce angular and linear acceleration of the head into velocity signals ( Fig. 9.5 ). ^, Three semicircular canals lie on each side of the head in three orthogonal planes that are approximately parallel to a mirror image set of planes on the contralateral side of the head. These canals are stimulated by brief angular rotations of the head and the resulting reflexive ocular rotation is referred to as the vestibulo-ocular reflex (angular VOR). In addition, two otoliths (the utricle and sacculus) transduce linear acceleration caused by head translation as well as head pitch (tilt about the interaural axis) and roll (tilt about the nasal–occipital axis) into translation velocity and head orientation signals (linear VOR). Angular acceleration signals stimulate the semicircular canals and result in eye rotations that are approximately equal and opposite to the motion of the head. This stabilization reflex has a short 7–15-msec latency because it is mediated by only three synapses and is accurate for head turns at velocities in excess of 300 deg/s. Hair cells in the canals can be stimulated by irrigation of one ear with cold water. This produces a caloric-vestibular nystagmus that causes the eyes to rotate slowly to the side of the irrigated ear. These slow-phase movements are interrupted by fast saccadic eye movements that reset eye position in the reverse direction (fast phase). A sequence of slow and fast phases is referred to as jerk nystagmus ( Fig. 9.6 ). Head rotations about horizontal, vertical, and nasal–occipital axes produce VOR responses with horizontal, vertical, and torsional counter-rotations of the slow phase of the nystagmus.

Figure 9.5, Vestibular end-organs in the human temporal bone. Three canals transduce angular head acceleration and two otoliths, the sacculus and utricle, transduce linear acceleration and head orientation. Right labyrinth and cochlea are viewed from horizontal aspect. (Drawings by Ernest W. Beck: courtesy Beltone Electronics Corp., Chicago, Ill.) The canals are in three orthogonal planes that are approximately parallel to a mirror image set of planes on the contralateral side of the head that lie roughly in the pulling direction of the three muscle planes. A, Lateral canals. B,C Anterior and posterior vertical canals. LC, lateral canal; AC anterior vertical canal: PC, posterior vertical canal.

Figure 9.6, OKN and VOR are composed of a slow phase (beta) that rotates the eye in a direction that stabilizes the retinal image and a fast phase (alpha) that resets the eye's position. The figure illustrates the vestibulo-ocular response to sustained rotation. The slow phase is in the direction opposite to head rotation. Horizontal position is plotted against time. The reflex gradually habituates and has disappeared by about 30 seconds.

To be effective, these reflex eye rotations must stabilize the retinal image. If the axis of angular head rotation coincided with the center of eye rotation, perfect compensation would occur if angular eye velocity equaled angular head velocity. However, the axis of head rotation is the neck and not the center of eye rotation such that when the head rotates, the eyes both rotate and translate with respect to the visual field. This is exacerbated during near viewing conditions. To stabilize the retinal image motion of a nearby target caused by angular head movements, the eye must rotate more than the head. Indeed, the gain of the VOR increases with convergence. Mismatches between eye and head velocity also occur with prescription spectacles that magnify or minify retinal image motion. Because the VOR responds directly to vestibular and not visual stimuli, its response is classified as open loop. The VOR compensates for visual errors by adapting its gain in response to retinal image slip to produce a stabilized retinal image. Perfect compensation would occur if angular eye velocity were equal and opposite to angular head velocity while viewing a distant scene. However empirical measures show that at high oscillation frequencies (2 Hz) compensation by the VOR is far from perfect and yet the world appears stable and single during rapid head shaking without any perceptual instability or oscillopsis. Thus, to perceive a stable world, the visual system must be aware of both the amount of head rotation and the inaccuracy of compensatory eye movements so that it can anticipate any residual retinal image motion during the head rotation.

Linear acceleration signals and gravity stimulate the otoliths and result in ocular rotations that are approximately 10 percent of the static head tilt caused by pitch and roll from vertical. Head pitch causes vertical eye rotations and head roll causes ocular torsion in the direction opposite to the head roll, “the ocular counterrolling reflex”. ^, Head roll can also elicit skew movements. When the otolith membranes are displaced on their maculae by inertial forces during rapid linear acceleration, such as during takeoff of an aircraft, a false sense of body pitch called the somatogravic illusion can occur. This illusion results from perceiving vertical as the non-vertical combination of gravitational and acceleration-inertial force vectors. The non-vertical gravitoinertial force causes pilots to perceive the aircraft as pitched upward during takeoff, and if the pilot corrects the false climb this can cause the aircraft nose to pitch downward with dangerous consequences.

Disorders of the vestibular system can produce imbalanced otolith inputs that can result in large amounts of vertical divergence of the eyes (skew deviation) by as much as 7 degrees, bilateral conjugate ocular torsion by as much as 25 degrees, and paradoxical head tilt known as the ocular tilt response (OTR). For example, if the head is tilted to the left, there is paradoxical torsion of both eyes in the direction of head roll and the left eye is rotated downward with respect to the right eye. Manifestations of the OTR will be discussed in the section on nystagmus.

B

Retinal signals

Head motion also produces whole-field retinal image motion of the visual field (optic flow). These retinal signals stimulate reflexive compensatory eye rotations that stabilize the retinal image during slow or long-lasting head movements. The eyes follow the moving field with a slow phase that is interrupted by resetting saccades (fast phase) 1 to 3 times per second. This jerk nystagmus is referred to as optokinetic nystagmus (OKN) and it complements the VOR by responding to low-velocity sustained head movements such as those that occur during walking and posture instability. Like the VOR, OKN also responds with horizontal, vertical and cyclo eye rotations to optic flow about vertical, horizontal, and nasal–occipital axes.

The optokinetic response to large fields has two components, including an early and delayed segment (OKNe and OKNd). OKNe is a short-latency ocular following response (<50 msec) that constitutes the rapid component of OKN, and OKNd builds up slowly after 7 seconds of stimulation. OKNe is likely to be mediated by the pursuit pathway. The delayed component is revealed by the continuation of OKNd in darkness (optokinetic after nystagmus, OKAN). OKNd results from a velocity memory or storage mechanism. ^, The time constant of the development of the OKAN matches the time constant of decay of the cupula in the semicircular canals. Thus OKAN builds up so that vision can compensate for loss of the vestibular inputs during prolonged angular rotation that might occur in a circular flight path. OKN can be used clinically to evaluate visual acuity objectively by measuring the smallest texture size and separation in a moving field that elicits the reflex.

C

Neuro-control of stabilization reflexes

1 Vestibulo-ocular reflex

The transducer that converts head rotation into a neural code for driving the VOR consists of a set of three semicircular canals paired on each side of the head. The horizontal canals are paired and the anterior canal on one side is paired with the posterior canal on the contralateral side ( Fig. 9.5 ). These are opponent pairs so that when one canal is stimulated by a given head rotation its paired member on the contralateral side is inhibited. For example, downward and forward head motion to the left causes increased firing of the vestibular nerve for the left anterior canal and decreased firing of the vestibular nerve projections from the right posterior canal. The three canals lie roughly in the pulling directions of the three muscle planes. Thus the left anterior canal and right posterior canal are parallel to the muscle planes of the left eye vertical recti and the right eye obliques. Pathways for the horizontal VOR are illustrated in Figure 9.7 for a leftward head rotation. Excitatory innervation projects from the left medial vestibular nucleus to the right abducens nucleus to activate the right lateral rectus, and an interneuron from the right abducens nucleus projects to the left oculomotor nucleus to activate the left medial rectus. The abducens serves as a premotor nucleus to coordinate conjugate horizontal movements to the ipsilateral side in accordance with Hering's law.

Figure 9.7, Pathways of the horizontal VOR in the brain stem for leftward head rotation. Inhibitory connections are shown as filled neurons, excitatory connections as unfilled neurons. Leftward head rotation stimulates the left horizontal canal and inhibits the right horizontal canal. This results in an increased discharge rate in the right lateral and left medial rectus and decreased discharge rate in the left lateral and right medial rectus. 31

The cerebellar flocculus is essential for adaptation of the VOR to optical distortions such as magnification. The flocculus receives excitatory inputs from retinal image motion (retinal slip) and head velocity information (canal signals) and inhibitory inputs from neural correlates of eye movements that provide a negative feedback signal. Adaptation only occurs if retinal image motion and head turns occur together. The gain of the VOR will be adapted to decrease whenever retinal slip and head turns are in the same direction, and to increase whenever they are in opposite directions. Following adaptation, an error correction signal is projected from the flocculus by Purkinje cells to floccular target neurons (FTN) in the vestibular nucleus to make appropriate changes in VOR gain.

2 You're Reading a Preview

Become a Clinical Tree membership for Full access and enjoy Unlimited articles

Become membership

If you are a member. Log in here