Comprehensive Physiology Wiley Online Library

Control of Eye Movements

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Purposes of eye Movements
1.1 Vestibuloocular Reflex
1.2 Afoveate Saccadic System
1.3 Optokinetic System
1.4 Visual Stabilization
1.5 Pursuit System
1.6 Saccadic System
1.7 Vergence System
2 Oculomotor Plant
2.1 Motoneuron Behavior
2.2 Movement and Muscle Fiber Types
2.3 Stretch Afferents
2.4 Muscle Mechanics
3 Vestibuloocular Reflex
3.1 Properties of Reflex
3.2 Semicircular Canals
3.3 Central Pathways
3.4 Otolith Reflex
3.5 Neurophysiology of Reflex
4 Optokinetic System
4.1 Properties of Optokinetic Nystagmus
4.2 Model of Optokinetic‐Vestibular Cooperation
4.3 Neurophysiology of Optokinetic System
5 Saccadic System
5.1 Properties of Rapid Eye Movements
5.2 Properties of Quick‐Phase System
5.3 Properties of Saccadic System
5.4 Neurophysiology of Saccades
6 Pursuit System
6.1 Stabilization System
6.2 Properties of Pursuit
6.3 Neurophysiology of Pursuit
6.4 Models of Pursuit
7 Vergence System
7.1 Properties of Vergence Movements
7.2 Neurophysiology of Vergence
8 Plasticity and Repair
8.1 Gain of Vestibuloocular Reflex
8.2 Recovery from VIIIth Nerve Lesions
8.3 Saccadic Plasticity
8.4 Plasticity of Vergence Tone
9 Measuring Eye Movements
9.1 Noncontact Methods
9.2 Contact Methods
Figure 1. Figure 1.

Examples of eye movements produced by various oculomotor subsystems. Time is indicated in seconds. A: the most common use of the vestibuloocular reflex is to stabilize eye position in space during a rapid eye‐head reorientation. The eye moves first in a saccade followed by a slower head movement (H) during which the eye rotates backward in the head (E) to compensate for head rotation and keep eye position in space, or gaze (G), fixed on new target. Data from monkey. B: nystagmus eye movements (E) in the cat produced by prolonged rotation in dark at a head velocity (H) of 20°/s. Slow phases have velocity of about 18°/s in compensatory direction. Note that quick phases keep eye shifted in direction of turning. C: optokinetic nystagmus in the rabbit. At zero time the drum begins rotating at 30°/s. Lines parallel to slow phases illustrate how slow‐phase eye velocity builds up slowly. D: eye drift in cat during fixation in light is shown (top trace). Mean drift velocity (estimated over 0.2‐s time intervals) is about 0.25°/s. Note lack of microsaccades. Eye drift increases in the dark (bottom trace). Sample record shows one velocity as high as 4°/s but 1°/s is typical Broken rapid movement is a large saccade. E: eye position (E) of trained monkey making smooth pursuit movement in response to target (T) moving in a ramp at 10°/s. Movement starts with a catch‐up saccade. F: eye position (E) of trained monkey making a saccade in response to a step of target position (T) of 10°. G: human convergence movement of 2° following a step in target position from far to near in midsaggital plane.

A from Miles and Fuller ; B from Robinson ; C from Collewijn ; D from Winterson and Robinson ; E, F from Fuchs ; G from Rashbass and Westheimer
Figure 2. Figure 2.

Behavior of eye muscle motoneurons in the monkey. A: during fixation (bottom trace), the rate of the discharges (top trace) is steady. B: rate varies linearly with fixation at different eye positions in the on‐ or off‐direction. Slope of rate‐position line is k. Intercept is the threshold ET. Four different cells (ad) illustrate high and low threshold units. Data points for 1 cell (b) illustrate variability. C: motoneuron discharges during pursuit. Discharge rate is much lower when eye passes through any given position travelling in off‐direction (first arrow) than when it returns travelling in on‐direction (second arrow). D: rate‐velocity curve. Rate varies as eye passes through given position (closed circles) in proportion to eye velocity (dE/dt) with proportionality factor r. E: rate‐velocity relationship seen most easily during saccades. Cells burst at high rates for on‐saccades (right) and pause for off‐saccades (left). F: rate‐velocity curves for several cells in both pursuit (<100°/s) and saccadic (>100°/s) velocity ranges show that eye velocity increases more rapidly than discharge rate.

AD from Robinson and Keller ; E, F from Robinson
Figure 3. Figure 3.

Mechanics of eye positioning. Top, family of solid curves show medial rectus (MR) force as a function of muscle length that is shown as equivalent eye rotation (E). Innervation is changed when patient looks straight ahead (0°) or to the left and right 15°, 30°, and 45° with the other eye. The amount of force exerted is measured in grams. Bottom, curves show similar lateral rectus (LR) length‐tension‐innervation curves. Force‐displacement relationship of passive orbital tissues is shown (–P curve). Dashed lines indicate sum of 2 muscle forces in attempted 0°, 15°, 30°, and 45° gaze in abduction (AB) and adduction (AD). The eye is at rest when dashed curves cross – P curve (filled circles), because sum of all forces is zero at that point. Dotted lines and open circles show operating locus of individual muscle's force as length and innervation change normally over the field of gaze. These curves allow one to know division of forces in orbit for any angle of gaze.

Some of the data in this figure from Collins
Figure 4. Figure 4.

Vestibuloocular reflex. See text for more complete explanation. A: Bode diagram of vestibuloocular reflex showing behavior of gain and phase with frequency. Heavy lines indicate overall behavior; dotted lines show contributions of various components. Effect of neural transformation II shown in Fig. C is to extend low‐frequency range over which reflex works properly from about 0.03 Hz (dashed curves marked Tc) to 0.01 Hz (using data from monkeys) as shown by solid curves. B: postrotatory nystagmus. When prolonged head rotation at constant velocity suddenly stops, cupula is displaced and returns with exponential time course with time constant Tc (curve marked cupula). Slow‐phase eye velocity decreases, however, with time constant Tvor, which is about 3 times larger than Tc (curve marked without adaptation). Adaptation alters this ideal curve by causing it to fall faster and by adding prolonged reversed tail. C: signal processing in reflex showing, in Laplace transform notation, transfer functions of sensory (canals), central, and motor (plant) parts of reflex in 4 stages (I–IV). Stage I describes the canals according to Equation . First step in central processing (stage II) is to convert main reflex time constant Tc to Tvor. When transfer functions I and II are multiplied, terms containing Tc cancel out and the result reflects effective cupula time constant of Tvor shown on the left in second row of equations. Next central step (III) is integrating velocity command (1/s) and compensating for plant lag by velocity feedforward path, Te1 (right equation, second line). Stage IV describes the plant as in Equation . Final transfer function (bottom line) is similar to that measured experimentally assuming that high‐frequency terms in brackets more or less cancel out. H, head position; , head velocity as coded by the canals; , a central signal that effects transformation II; Rv1, discharge rate of primary vestibular neurons; Rv2, discharge rate of second‐order vestibular neurons; , central head velocity signal; , vestibular eye velocity command; E, eye position; NI, neural integrator; Rm, discharge rate of motoneurons; −g, overall reflex gain.

Figure 5. Figure 5.

Schematic of major pathways and signals mediating vestibuloocular reflex. A head velocity signal ( ) is relayed from horizontal (hc) and vertical canals (vc) by the discharge rate (Rv1) of primary vestibular afferents to tonic‐vestibular‐pause cells (TVP) in the vestibular nucleus (VN). Excitatory cells are indicated by open circles, inhibitory cells by filled circles. Excitatory vertical reflex is relayed via discharge rate Rtvp of TVP fibers in the contralateral medial longitudinal fasciculus (MLF) to motoneurons of vertical muscles (vm) in the oculomotor nucleus (III). Eye position (E) and eye velocity commands ( , ) are added both at level of VN and motoneurons. It is hypothesized that the horizontal reflex is also mediated by TVP fibers projecting to lateral rectus (lr) motoneurons in abducens nucleus (VI) and relayed to medial rectus (mr) motoneurons via internuclear neurons (IN) in VI. Dashed line, eye position signals of 1.5E and 2.5E may come from tonic cells (T) in neural integrator (NI). Equations for signals Rv1, Rtvp, Rbt, and Rm are explained in text. Inhibitory cells for vertical reflex lie in superior vestibular nucleus (SVN) and ascend in ipsilateral MLF. Other excitatory and inhibitory fibers appear to lie in rostral medial VN (RMVN). B, burst cells; Rbt, burst‐tonic signal; –| |, pause created by inhibitory burst cells; Rm, motoneuron signal.

Figure 6. Figure 6.

A: saggital section of the monkey brain stem showing the region (stippled) in which lesions cause severe deficits in eye movements and which is now loosely called the paramedian pontine reticular formation (PPRF). Brach conj, brachium conjunctivum; Inf coll, inferior colliculus; Inf olive, inferior olive; MLF, medial longitudinal fasciculus; N fast, fastigial nucleus; N ret mag, nucleus reticularis magnocellularis; N teg vent, nucleus tegmenti ventralis; Post comm, posterior commissure; Sup coll, superior colliculus; III, oculomotor; IV, trochlear, and VI, abducens nucleus. B: cross section of the monkey brain stem, cut in stereotaxic vertical (see slant line top left in A for orientation) in a plane just posterior to the trochlear nucleus and just anterior to the abducens nucleus. Lined region is the PPRF. PT, pyramidal tract; Pulv, pulvinar; SO, superior olive; SC, superior colliculus; VI, abducens nerve rootlets.

A from Goebels et al. ; B from Cohen and Komatsuzaki
Figure 7. Figure 7.

Time course of optokinetic nystagmus for 4 species. A: when animal rotates in light at constant velocity (left), vestibular signal (V), as a function of time, falls back to zero, whereas optokinetic eye velocity command (OK) rises with a complementary time course. The sum provides an eye velocity command (heavy line) that compensates for head velocity for both transient and sustained parts of rotation. When rotation stops (right) optokinetic and vestibular signals cancel and the eye comes to rest. B: when an optokinetic drum starts to rotate at velocity about a stationary animal, eye velocity jumps to initial value and then rises slowly with time constant Tok to a steady‐state value . When lights are turned out (vertical arrow) eye velocity falls quickly to the level and then falls back to zero slowly with time constant Tokan. C: values of characteristic constants for optokinetic nystagmus in deg/s, percent, or seconds, for 4 species at typical drum speeds. Note Tokan for cat is small because this animal has a pronounced optokinetic after‐afternystagmus that was not taken into account.

B, C species data obtained from the following sources: human being from B. Cohen and V. Henn, unpublished observations; monkey from Cohen et al. ; cat from Haddad et al. ; rabbit from Collewijn
Figure 8. Figure 8.

Schematic representation of optokinetic system. For pure optokinetic stimulation W (head velocity equal to zero), a storage element S accumulates a signal due to retinal slip and produces an output that appears in vestibular nucleus (VN). Transfer function between retinal slip and eye velocity command (above) is characterized by a gain Gok and a long time constant Tokan that accounts for OKAN. Same storage element also can account for the long time constant Tvor of rotatory nystagmus in dark as shown by transfer function between the canal signal and (right). Element S can achieve this behavior by receiving either a direct canal input via the feedforward pathway (ff) or a feedback pathway (fb) from the eye velocity signal. See text for detailed explanation. , eye velocity in the head; f( ), nonlinearity in visual pathway; , velocity of eye in space; S1, switch that removes all retinal input in the dark; Tc, cupula time constant.

Figure 9. Figure 9.

Relationship between peak saccadic eye velocity and saccade amplitude. Curve Bg comes from study that surveyed population of human subjects. Shaded area indicates normal limits for mean velocities of individual subjects in that study.

Data for human saccades obtained from the following sources: curve Bh from Bahill et al. ; curve W from Westheimer ; curve Bg from Boghen et al. . Animal data obtained from following sources: curve M (monkey) from Fuchs ; curve F (goldfish) from Easter ; curve C (cat) from Crommelinck and Roucoux
Figure 10. Figure 10.

Push‐pull arrangement by which burst cells create saccades. Ipsilateral burst cells (Bi) discharge at high rates (Rb) during leftward saccades. They excite ipsilateral abducens motoneurons in abducens nucleus (VI) and relay an inhibitory burst through B′i, located in ipsilateral rostral medulla, to burst‐tonic, internuclear neurons (IN) in contralateral VI, which fire at rate Rbt. This inhibitory burst silences contralateral IN cells and ipsilateral medial rectus motoneurons in oculomotor nucleus (III) during the saccade. Burst rate (Rm) in lateral rectus motoneuron is difference between rates Rh of Bi and that of contralateral inhibitory cells B′c relayed from contralateral burst cells Bc. Neural integrator (NI) must be formed by a pair of reciprocally acting circuits in paramedian pontine reticular formation with midline symmetry. They are represented by tonic cells (T) and must also be stepped up or down (discharge rates Rt) by the push‐pull action of burst cells to produce the final pulse‐step Rm (or pause‐step Rbt) in agonist (or antagonist) motoneurons. Closed circles, inhibitory cells; open circles, excitatory cells.

Figure 11. Figure 11.

Hering's law for mixed conjugate and vergence movements and violations of that law. A: schematic diagram shows how intersection of visual axes gets from A to D (arrows) with combined vergence and conjugate movement according to modified Hering's law. B: example of a special case of the situation in A. Two targets are aligned on the axis of one eye, the left eye in this case. Left eye (LE) makes a combined saccade and divergence movement with no net displacement. Hering's law is approximately obeyed although saccade in the right eye (RE) is clearly half again as big as that in the left eye. C: example in which Hering's law is grossly disobeyed. This shows a case of symmetric divergence in which near and far targets lie in a midsaggital plane. Initial saccade of the left eye is much larger than that of the right eye; opposite is true for vergence movements.

B from Riggs and Niehl ; C from Clark and Crane
Figure 12. Figure 12.

Plastic adaptation of gain of vestibuloocular reflex. A: one hypothesis for adaptation is that output of semicircular canal (SCC) projects directly to vestibular nucleus (VN) with gain α and indirectly on mossy fibers (mf), granule cells (gc), parallel T‐fibers, and Purkinje cells (Pc) in the vestibulocerebellum (VC) with gain β. Retinal image slip signal projects from retina through nucleus of optic tract (not) and inferior olive (IO) to Purkinje cells (Pc) on climbing fibers (cf). If cf activity could change mf‐Pc synaptic gain β, gain of the entire reflex could be changed to eliminate retinal slip during head movements. , eye velocity; , head velocity; OMN, oculomotor nucleus. B: filled circles and solid line show that gain of reflex is driven from about 0.9 (left) down to about 0.1 in 8 days after cats begin to wear reversing prisms chronically (arrow). Crosses and dashed line show that after vestibulocerebellectomy (crblx) gain can no longer be modified by wearing reversing prisms.

From Robinson
Figure 13. Figure 13.

Saccadic plasticity. A monkey is trained to follow a spot that jumps, in this example, by 10°. A: its left eye is weakened by tenectomy and patched. That eye subsequently makes hypometric saccades one‐third as large as those of the normal eye and with a backward postsaccadic slip (top left). B: 3 days after switching the patch, weakened eye has regained ability to make orthometric saccades, while the good eye, under cover, makes hypermetric saccades with postsaccadic slip in opposite direction (bottom right). This demonstrates that central nervous system can repair dysmetria (created by a peripheral lesion) in this case by increasing gain (saccade size/retinal error) of central part of saccadic system.

From Optican and Robinson


Figure 1.

Examples of eye movements produced by various oculomotor subsystems. Time is indicated in seconds. A: the most common use of the vestibuloocular reflex is to stabilize eye position in space during a rapid eye‐head reorientation. The eye moves first in a saccade followed by a slower head movement (H) during which the eye rotates backward in the head (E) to compensate for head rotation and keep eye position in space, or gaze (G), fixed on new target. Data from monkey. B: nystagmus eye movements (E) in the cat produced by prolonged rotation in dark at a head velocity (H) of 20°/s. Slow phases have velocity of about 18°/s in compensatory direction. Note that quick phases keep eye shifted in direction of turning. C: optokinetic nystagmus in the rabbit. At zero time the drum begins rotating at 30°/s. Lines parallel to slow phases illustrate how slow‐phase eye velocity builds up slowly. D: eye drift in cat during fixation in light is shown (top trace). Mean drift velocity (estimated over 0.2‐s time intervals) is about 0.25°/s. Note lack of microsaccades. Eye drift increases in the dark (bottom trace). Sample record shows one velocity as high as 4°/s but 1°/s is typical Broken rapid movement is a large saccade. E: eye position (E) of trained monkey making smooth pursuit movement in response to target (T) moving in a ramp at 10°/s. Movement starts with a catch‐up saccade. F: eye position (E) of trained monkey making a saccade in response to a step of target position (T) of 10°. G: human convergence movement of 2° following a step in target position from far to near in midsaggital plane.

A from Miles and Fuller ; B from Robinson ; C from Collewijn ; D from Winterson and Robinson ; E, F from Fuchs ; G from Rashbass and Westheimer


Figure 2.

Behavior of eye muscle motoneurons in the monkey. A: during fixation (bottom trace), the rate of the discharges (top trace) is steady. B: rate varies linearly with fixation at different eye positions in the on‐ or off‐direction. Slope of rate‐position line is k. Intercept is the threshold ET. Four different cells (ad) illustrate high and low threshold units. Data points for 1 cell (b) illustrate variability. C: motoneuron discharges during pursuit. Discharge rate is much lower when eye passes through any given position travelling in off‐direction (first arrow) than when it returns travelling in on‐direction (second arrow). D: rate‐velocity curve. Rate varies as eye passes through given position (closed circles) in proportion to eye velocity (dE/dt) with proportionality factor r. E: rate‐velocity relationship seen most easily during saccades. Cells burst at high rates for on‐saccades (right) and pause for off‐saccades (left). F: rate‐velocity curves for several cells in both pursuit (<100°/s) and saccadic (>100°/s) velocity ranges show that eye velocity increases more rapidly than discharge rate.

AD from Robinson and Keller ; E, F from Robinson


Figure 3.

Mechanics of eye positioning. Top, family of solid curves show medial rectus (MR) force as a function of muscle length that is shown as equivalent eye rotation (E). Innervation is changed when patient looks straight ahead (0°) or to the left and right 15°, 30°, and 45° with the other eye. The amount of force exerted is measured in grams. Bottom, curves show similar lateral rectus (LR) length‐tension‐innervation curves. Force‐displacement relationship of passive orbital tissues is shown (–P curve). Dashed lines indicate sum of 2 muscle forces in attempted 0°, 15°, 30°, and 45° gaze in abduction (AB) and adduction (AD). The eye is at rest when dashed curves cross – P curve (filled circles), because sum of all forces is zero at that point. Dotted lines and open circles show operating locus of individual muscle's force as length and innervation change normally over the field of gaze. These curves allow one to know division of forces in orbit for any angle of gaze.

Some of the data in this figure from Collins


Figure 4.

Vestibuloocular reflex. See text for more complete explanation. A: Bode diagram of vestibuloocular reflex showing behavior of gain and phase with frequency. Heavy lines indicate overall behavior; dotted lines show contributions of various components. Effect of neural transformation II shown in Fig. C is to extend low‐frequency range over which reflex works properly from about 0.03 Hz (dashed curves marked Tc) to 0.01 Hz (using data from monkeys) as shown by solid curves. B: postrotatory nystagmus. When prolonged head rotation at constant velocity suddenly stops, cupula is displaced and returns with exponential time course with time constant Tc (curve marked cupula). Slow‐phase eye velocity decreases, however, with time constant Tvor, which is about 3 times larger than Tc (curve marked without adaptation). Adaptation alters this ideal curve by causing it to fall faster and by adding prolonged reversed tail. C: signal processing in reflex showing, in Laplace transform notation, transfer functions of sensory (canals), central, and motor (plant) parts of reflex in 4 stages (I–IV). Stage I describes the canals according to Equation . First step in central processing (stage II) is to convert main reflex time constant Tc to Tvor. When transfer functions I and II are multiplied, terms containing Tc cancel out and the result reflects effective cupula time constant of Tvor shown on the left in second row of equations. Next central step (III) is integrating velocity command (1/s) and compensating for plant lag by velocity feedforward path, Te1 (right equation, second line). Stage IV describes the plant as in Equation . Final transfer function (bottom line) is similar to that measured experimentally assuming that high‐frequency terms in brackets more or less cancel out. H, head position; , head velocity as coded by the canals; , a central signal that effects transformation II; Rv1, discharge rate of primary vestibular neurons; Rv2, discharge rate of second‐order vestibular neurons; , central head velocity signal; , vestibular eye velocity command; E, eye position; NI, neural integrator; Rm, discharge rate of motoneurons; −g, overall reflex gain.



Figure 5.

Schematic of major pathways and signals mediating vestibuloocular reflex. A head velocity signal ( ) is relayed from horizontal (hc) and vertical canals (vc) by the discharge rate (Rv1) of primary vestibular afferents to tonic‐vestibular‐pause cells (TVP) in the vestibular nucleus (VN). Excitatory cells are indicated by open circles, inhibitory cells by filled circles. Excitatory vertical reflex is relayed via discharge rate Rtvp of TVP fibers in the contralateral medial longitudinal fasciculus (MLF) to motoneurons of vertical muscles (vm) in the oculomotor nucleus (III). Eye position (E) and eye velocity commands ( , ) are added both at level of VN and motoneurons. It is hypothesized that the horizontal reflex is also mediated by TVP fibers projecting to lateral rectus (lr) motoneurons in abducens nucleus (VI) and relayed to medial rectus (mr) motoneurons via internuclear neurons (IN) in VI. Dashed line, eye position signals of 1.5E and 2.5E may come from tonic cells (T) in neural integrator (NI). Equations for signals Rv1, Rtvp, Rbt, and Rm are explained in text. Inhibitory cells for vertical reflex lie in superior vestibular nucleus (SVN) and ascend in ipsilateral MLF. Other excitatory and inhibitory fibers appear to lie in rostral medial VN (RMVN). B, burst cells; Rbt, burst‐tonic signal; –| |, pause created by inhibitory burst cells; Rm, motoneuron signal.



Figure 6.

A: saggital section of the monkey brain stem showing the region (stippled) in which lesions cause severe deficits in eye movements and which is now loosely called the paramedian pontine reticular formation (PPRF). Brach conj, brachium conjunctivum; Inf coll, inferior colliculus; Inf olive, inferior olive; MLF, medial longitudinal fasciculus; N fast, fastigial nucleus; N ret mag, nucleus reticularis magnocellularis; N teg vent, nucleus tegmenti ventralis; Post comm, posterior commissure; Sup coll, superior colliculus; III, oculomotor; IV, trochlear, and VI, abducens nucleus. B: cross section of the monkey brain stem, cut in stereotaxic vertical (see slant line top left in A for orientation) in a plane just posterior to the trochlear nucleus and just anterior to the abducens nucleus. Lined region is the PPRF. PT, pyramidal tract; Pulv, pulvinar; SO, superior olive; SC, superior colliculus; VI, abducens nerve rootlets.

A from Goebels et al. ; B from Cohen and Komatsuzaki


Figure 7.

Time course of optokinetic nystagmus for 4 species. A: when animal rotates in light at constant velocity (left), vestibular signal (V), as a function of time, falls back to zero, whereas optokinetic eye velocity command (OK) rises with a complementary time course. The sum provides an eye velocity command (heavy line) that compensates for head velocity for both transient and sustained parts of rotation. When rotation stops (right) optokinetic and vestibular signals cancel and the eye comes to rest. B: when an optokinetic drum starts to rotate at velocity about a stationary animal, eye velocity jumps to initial value and then rises slowly with time constant Tok to a steady‐state value . When lights are turned out (vertical arrow) eye velocity falls quickly to the level and then falls back to zero slowly with time constant Tokan. C: values of characteristic constants for optokinetic nystagmus in deg/s, percent, or seconds, for 4 species at typical drum speeds. Note Tokan for cat is small because this animal has a pronounced optokinetic after‐afternystagmus that was not taken into account.

B, C species data obtained from the following sources: human being from B. Cohen and V. Henn, unpublished observations; monkey from Cohen et al. ; cat from Haddad et al. ; rabbit from Collewijn


Figure 8.

Schematic representation of optokinetic system. For pure optokinetic stimulation W (head velocity equal to zero), a storage element S accumulates a signal due to retinal slip and produces an output that appears in vestibular nucleus (VN). Transfer function between retinal slip and eye velocity command (above) is characterized by a gain Gok and a long time constant Tokan that accounts for OKAN. Same storage element also can account for the long time constant Tvor of rotatory nystagmus in dark as shown by transfer function between the canal signal and (right). Element S can achieve this behavior by receiving either a direct canal input via the feedforward pathway (ff) or a feedback pathway (fb) from the eye velocity signal. See text for detailed explanation. , eye velocity in the head; f( ), nonlinearity in visual pathway; , velocity of eye in space; S1, switch that removes all retinal input in the dark; Tc, cupula time constant.



Figure 9.

Relationship between peak saccadic eye velocity and saccade amplitude. Curve Bg comes from study that surveyed population of human subjects. Shaded area indicates normal limits for mean velocities of individual subjects in that study.

Data for human saccades obtained from the following sources: curve Bh from Bahill et al. ; curve W from Westheimer ; curve Bg from Boghen et al. . Animal data obtained from following sources: curve M (monkey) from Fuchs ; curve F (goldfish) from Easter ; curve C (cat) from Crommelinck and Roucoux


Figure 10.

Push‐pull arrangement by which burst cells create saccades. Ipsilateral burst cells (Bi) discharge at high rates (Rb) during leftward saccades. They excite ipsilateral abducens motoneurons in abducens nucleus (VI) and relay an inhibitory burst through B′i, located in ipsilateral rostral medulla, to burst‐tonic, internuclear neurons (IN) in contralateral VI, which fire at rate Rbt. This inhibitory burst silences contralateral IN cells and ipsilateral medial rectus motoneurons in oculomotor nucleus (III) during the saccade. Burst rate (Rm) in lateral rectus motoneuron is difference between rates Rh of Bi and that of contralateral inhibitory cells B′c relayed from contralateral burst cells Bc. Neural integrator (NI) must be formed by a pair of reciprocally acting circuits in paramedian pontine reticular formation with midline symmetry. They are represented by tonic cells (T) and must also be stepped up or down (discharge rates Rt) by the push‐pull action of burst cells to produce the final pulse‐step Rm (or pause‐step Rbt) in agonist (or antagonist) motoneurons. Closed circles, inhibitory cells; open circles, excitatory cells.



Figure 11.

Hering's law for mixed conjugate and vergence movements and violations of that law. A: schematic diagram shows how intersection of visual axes gets from A to D (arrows) with combined vergence and conjugate movement according to modified Hering's law. B: example of a special case of the situation in A. Two targets are aligned on the axis of one eye, the left eye in this case. Left eye (LE) makes a combined saccade and divergence movement with no net displacement. Hering's law is approximately obeyed although saccade in the right eye (RE) is clearly half again as big as that in the left eye. C: example in which Hering's law is grossly disobeyed. This shows a case of symmetric divergence in which near and far targets lie in a midsaggital plane. Initial saccade of the left eye is much larger than that of the right eye; opposite is true for vergence movements.

B from Riggs and Niehl ; C from Clark and Crane


Figure 12.

Plastic adaptation of gain of vestibuloocular reflex. A: one hypothesis for adaptation is that output of semicircular canal (SCC) projects directly to vestibular nucleus (VN) with gain α and indirectly on mossy fibers (mf), granule cells (gc), parallel T‐fibers, and Purkinje cells (Pc) in the vestibulocerebellum (VC) with gain β. Retinal image slip signal projects from retina through nucleus of optic tract (not) and inferior olive (IO) to Purkinje cells (Pc) on climbing fibers (cf). If cf activity could change mf‐Pc synaptic gain β, gain of the entire reflex could be changed to eliminate retinal slip during head movements. , eye velocity; , head velocity; OMN, oculomotor nucleus. B: filled circles and solid line show that gain of reflex is driven from about 0.9 (left) down to about 0.1 in 8 days after cats begin to wear reversing prisms chronically (arrow). Crosses and dashed line show that after vestibulocerebellectomy (crblx) gain can no longer be modified by wearing reversing prisms.

From Robinson


Figure 13.

Saccadic plasticity. A monkey is trained to follow a spot that jumps, in this example, by 10°. A: its left eye is weakened by tenectomy and patched. That eye subsequently makes hypometric saccades one‐third as large as those of the normal eye and with a backward postsaccadic slip (top left). B: 3 days after switching the patch, weakened eye has regained ability to make orthometric saccades, while the good eye, under cover, makes hypermetric saccades with postsaccadic slip in opposite direction (bottom right). This demonstrates that central nervous system can repair dysmetria (created by a peripheral lesion) in this case by increasing gain (saccade size/retinal error) of central part of saccadic system.

From Optican and Robinson
References
 1. Abel, L. A., D. Schmidt, L. F. Dell'Osso, and R. B. Daroff. Saccadic system plasticity in humans. Ann. Neurol. 4: 313–318, 1978.
 2. Abend, W. K. Functional organization of the superior vestibular nucleus of the squirrel monkey. Brain Res. 132: 65–84, 1977.
 3. Abrahams, V. C., F. Richmond, and P. K. Rose. Basic physiology of the head‐eye movement system. In: Basic Mechanisms of Ocular Motility and Their Clinical Implications, edited by G. Lennerstrand and P. Bach‐y‐Rita. Oxford: Pergamon, 1975, vol. 24, p. 473–476. (Wenner‐Gren Cent. Int. Symp. Ser.).
 4. Alley, K. A., Anatomical basis for interaction between cerebellar flocculus and brainstem. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, p. 109–117.
 5. Alpern, M., Movements of the eyes. In: The Eye, edited by H. Davson. New York: Academic, 1962, vol. 3, p. 91–93.
 6. Alvarado, J. A., and C. Van Horn. Muscle cell types of the cat inferior oblique. In: Basic Mechanisms of Ocular Motility and Their Clinical Implications, edited by G. Lennerstrand and P. Bach‐y‐Rita. Oxford: Pergamon, 1975, vol. 24, p. 15–43. (Wenner‐Green Cent. Int. Symp. Ser.).
 7. Alvarado‐Mallart, R. M., C. Buisseret‐Delmas, J. F. Gueritaud, and G. Horcholle‐Bossavit. Primary mesencephalic projections of the rectus lateralis muscle afferents in cat: Physiological and anatomical evidence. In: Basic Mechanisms of Ocular Motility and Their Clinical Implications, edited by G. Lennerstrand and P. Bach‐y‐Rita. Oxford: Pergamon, 1975, vol. 24, p. 465–468. (Wenner‐Gren Cent. Int. Symp. Ser.).
 8. Baarsma, E. A., and H. Collewijn. Vestibulo‐ocular and optokinetic reactions to rotation and their interaction in the rabbit. J. Physiol. London 238: 603–625, 1974.
 9. Baarsma, E. A., and H. Collewijn. Eye movements due to linear accelerations in the rabbit. J. Physiol. London 245: 227–247, 1975.
 10. Bach‐y‐Rita, P. Structural‐functional correlations in eye muscle fibers. Eye muscle proprioception. In: Basic Mechanisms of Ocular Motility and Their Clinical Implications, edited by G. Lennerstrand and P. Bach‐y‐Rita. Oxford: Pergamon, 1975, vol. 24, p. 91–111. (Wenner‐Gren Cent. Int. Symp. Ser.).
 11. Bach‐y‐Rita, P., and F. Ito. In vivo studies on fast and slow muscle fibers in cat extraocular muscles. J. Gen. Physiol. 49: 1177–1198, 1966.
 12. Bahill, A. T., K. A. Bahill, M. R. Clark, and L. Stark. Closely spaced saccades. Invest. Ophthalmol. 14: 317–320, 1975.
 13. Bahill, A. T., K. J. Ciuffreda, R. Kenyon, and L. Stark. Dynamic and static violations of Hering's law of equal innervation. Am. J. Optom. Physiol. Opt. 53: 786–796, 1977.
 14. Bahill, A. T., M. R. Clark, and L. Stark. Dynamic overshoot in saccadic eye movements is caused by neurological control signal reversals. Exp. Neurol. 48: 107–122, 1975.
 15. Bahill, A. T., M. R. Clark, and L. Stark. Glissades‐eye movements generated by mismatched components of the saccadic motoneuronal control signal. Math. Biosci. 26: 303–318, 1975.
 16. Bahill, A. T., M. R. Clark, and L. Stark. The main sequence, a tool for studying human eye movements. Math. Biosci. 24: 191–204, 1975.
 17. Baker, R., The nucleus prepositus hypoglossi. In: Eye Movements, edited by B. A. Brooks and F. J. Bajandas, New York: Plenum, 1977, p. 145–178, (ARVO Symp., 1976.).
 18. Baker, R., and A. Berthoz. Organization of vestibular nystagmus in oblique oculomotor system. J. Neurophysiol. 37: 195–217, 1974.
 19. Baker, R., and S. M. Highstein. Vestibular projections to medial rectus subdivision of oculomotor nucleus. J. Neurophysiol. 41: 1629–1646, 1978.
 20. Baker, R., and W. Precht. Electrophysiological properties of trochlear motoneurons as revealed by IV nerve stimulation. Exp. Brain Res. 14: 127–157, 1972.
 21. Baker, R., W. Precht, and R. Llinás. Mossy and climbing fiber projections of extraocular muscle afferents to the cerebellum. Brain Res. 38: 440–445, 1972.
 22. Barmack, N. H., Visually evoked activity of neurons in the dorsal cap of the inferior olive and its relationship to the control of eye movements. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, p. 361–370.
 23. Barnes, G. R. The role of the vestibulo‐ocular reflex in visual target acquisition. J. Physiol. London 258: 64P–65P, 1976.
 24. Barr, C. C., L. W. Schultheis, and D. A. Robinson. Voluntary, non‐visual control of the human vestibuloocular reflex. Acta Oto‐Laryngol. 81: 365–375, 1976.
 25. Becker, W., and A. F. Fuchs. Further properties of the human saccadic system: eye movements and correction saccades with and without visual fixation points. Vision Res. 9: 1247–1258, 1969.
 26. Becker, W., and R. Jürgens. Saccadic reactions to double‐step stimuli: evidence for model feedback and continuous information uptake. In: Basic Mechanisms of Ocular Motility and Their Clinical Implications, edited by G. Lennerstrand and P. Bach‐y‐Rita. Oxford: Pergamon, 1975, vol. 24, p. 519–524. (Wenner‐Gren Cent. Int. Symp. Ser.).
 27. Becker, W., and R. Jürgens. An analysis of the saccadic system by means of double step stimuli. Vision Res. 19: 967–983, 1979.
 28. Becker, W., and H. M. Klein. Accuracy of saccadic eye movements and maintenance of eccentric eye positions in the dark. Vision Res. 13: 1021–1034, 1973.
 29. Bender, M. B. The oculomotor decussation. Am. J. Ophthalmol. 54: 591–596, 1962.
 30. Bender, M. B., and S. Shanzer. Oculomotor pathways defined by electric stimulation and lesions in the brain stem of monkey. In: Oculomotor System, edited by M. B. Bender. New York: Harper & Row, 1964, p. 81–140.
 31. Benson, A. J., Interactions between semi‐circular canals and gravireceptors. In: Recent Advances in Aerospace Medicine: Proceedings, edited by D. E. Busby. Dordrecht: Reidel, 1970, p. 249–261. (Int. Congr. Aviat. Space Med., 18th, Amsterdam, 1969.).
 32. Bishop, P. O., Neurophysiology of binocular single vision and stereopsis. In: Handbook of Sensory Physiology. Central Processing of Visual Information, edited by R. Jung. New York: Springer‐Verlag, 1973, vol. VII, pt. 3, p. 255–305.
 33. Bizzi, E. Discharge of frontal eye field neurons during saccadic and following eye movements in unanesthetized monkeys. Exp. Brain Res. 6: 69–80, 1968.
 34. Boghen, D., B. T. Troost, R. B. Daroff, L. F. Dell'Osso, and J. E. Birkett. Velocity characteristics of normal human saccades. Invest. Ophthalmol. 13: 619–623, 1974.
 35. Bond, H. W., and P. Ho. Solid miniature silver‐silver chloride electrodes for chronic implantation. Electroencephalogr. Clin. Neurophysiol. 28: 206–208, 1970.
 36. ter Braak, J. W. G., V. W. D. Schenk, and A. G. M. Van Vliet. Visual reactions in a case of long‐lasting cortical blindness. J. Neurol. Neurosurg. Psychiatry 34: 140–147, 1971.
 37. Brandt, T., J. Dichgans, and W. Büchele. Motion habituation: inverted self‐motion perception and optokinetic after‐nystagmus. Exp. Brain Res. 21: 337–352, 1974.
 38. Brandt, T., J. Dichgans, and E. Koenig. Differential effects of central versus peripheral vision on egocentric and exocentric motion perception. Exp. Brain Res. 16: 476–491, 1973.
 39. Brodal, A., Anatomy of the vestibular nuclei and their connections. In: Handbook of Sensory Physiology. Vestibular System, edited by H. H. Kornhuber. Berlin: Springer‐Verlag, 1974, vol. VI, pt. 1, p. 239–352.
 40. Buettner, U. W., U. Büttner, and V. Henn. Transfer characteristics of neurons in vestibular nuclei of the alert monkey. J. Neurophysiol. 41: 1614–1628, 1978.
 41. Buisseret, P., and L. Maffei. Extraocular proprioceptive projections to the visual cortex. Exp. Brain Res. 28: 421–425, 1977.
 42. Büttner, U., J. A. Büttner‐Ennever, and V. Henn. Vertical eye movement related unit activity in the rostral mesencephalic reticular formation of the alert monkey. Brain Res. 130: 239–252, 1977.
 43. Büttner‐Ennever, J. A., and U. Büttner. A cell group associated with vertical eye movements in the rostral mesencephalic reticular formation of the monkey. Brain Res. 151: 31–47, 1978.
 44. Byford, G. H. Non‐linear relations between the corneo‐retinal potential and horizontal eye movements. J. Physiol. London 168: 14P–15P, 1963.
 45. Carpenter, M. B., Central oculomotor pathways. In: Control of Eye Movements, edited by P. Bach‐y‐Rita and C. C. Collins. New York: Academic, 1971, p. 67–103.
 46. Carpenter, R. H. S. Movements of the Eyes. London: Pion, 1977.
 47. Cazin, L., W. Precht, and J. Lannou. Pathways mediating optokinetic responses of vestibular nucleus neurons in the rat. Pfluegers Arch. 384: 19–29, 1980.
 48. Chun, K.‐S., and D. A. Robinson. A model of quick phase generation in the vestibuloocular reflex. Biol. Cybernet. 28: 209–221, 1978.
 49. Clark, M. R., and H. D. Crane. Dynamic interactions in binocular vision. In: Eye Movements and the Higher Psychological Functions, edited by J. W. Senders, D. F. Fisher, and R. A. Monty. New York: Halsted, 1978, p. 77–88.
 50. Clark, M. R., and L. Stark. Control of human eye movements: I. Modelling of extraocular muscles; II. A model for the extraocular plant mechanism; III. Dynamic characteristics of the eye tracking mechanism. Math. Biosci. 20: 191–265, 1974.
 51. Close, R. I., and A. R. Luff. Dynamic properties of inferior rectus muscle of the rat. J. Physiol. London 236: 259–270, 1974.
 52. Cohen, B., and V. Henn. Unit activity in the pontine reticular formation associated with eye movements. Brain Res. 46: 403–410, 1972.
 53. Cohen, B., V. Henn, and L. R. Young. Visual‐vestibular interaction in motion perception and the generation of nystagmus. Neurosci. Res. Program Bull. In press.
 54. Cohen, B., and A. Komatsuzaki. Eye movements induced by stimulation of the pontine reticular formation: evidence for integration in oculomotor pathways. Exp. Neurol. 36: 101–117, 1972.
 55. Cohen, B., V. Matsuo, and T. Raphan. Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic after‐nystagmus. J. Physiol. London 270: 321–344, 1977.
 56. Collewijn, H. Optokinetic eye movements in the rabbit: input‐output relations. Vision Res. 9: 117–132, 1969.
 57. Collewijn, H. Dysmetria of fast phase of optokinetic nystagmus in cerebellectomized rabbits. Exp. Neurol. 28: 144–154, 1970.
 58. Collewijn, H. The normal range of horizontal eye movements in the rabbit. Exp. Neurol. 28: 132–143, 1970.
 59. Collewijn, H. An analog model of the rabbit's optokinetic system. Brain Res. 36: 71–88, 1972.
 60. Collewijn, H. Latency and gain of the rabbit's optokinetic reactions to small movements. Brain Res. 36: 59–70, 1972.
 61. Collewijn, H. Oculomotor areas in the rabbit's brain stem. Brain Res. 66: 362–363, 1974.
 62. Collewijn, H. Direction selective units in the rabbit's nucleus of the optic tract. Brain Res. 100: 489–508, 1975.
 63. Collewijn, H. Impairment of optokinetic (after‐) nystagmus by labyrinthectomy in the rabbit. Exp. Neurol. 52: 146–156, 1976.
 64. Collewijn, H. Eye and head movements in freely moving rabbits. J. Physiol. London 266: 471–498, 1977.
 65. Collewijn, H. Optokinetic and vestibulo‐ocular reflexes in dark‐reared rabbits. Exp. Brain Res. 27: 287–300, 1977.
 66. Collewijn, H., and F. Van der Mark. Ocular stability in variable visual feedback conditions in the rabbit. Brain Res. 36: 47–57, 1972.
 67. Collewijn, H., F. Van der Mark, and T. C. Jansen. Precise recording of human eye movements. Vision Res. 15: 447–450, 1975.
 68. Collewijn, H., B. J. Winterson, and M. F. W. Dubois. Optokinetic eye movements in albino rabbits: inversion in anterior visual field. Science 199: 1351–1353, 1978.
 69. Collins, C. C., Orbital mechanics. In: Control of Eye Movements, edited by P. Bach‐y‐Rita and C. C. Collins. New York: Academic, 1971, p. 283–326.
 70. Collins, C. C., The human oculomotor control system. In: Basic Mechanisms of Ocular Motility and Their Clinical Implications, edited by G. Lennerstrand and P. Bach‐y‐Rita. Oxford: Pergamon, 1975, vol. 24, p. 145–180. (Wenner‐Gren Cent. Int. Symp. Ser.).
 71. Collins, W. E. Effects of mental set upon vestibular nystagmus. J. Exp. Psychol. 63: 191–197, 1962.
 72. Cooper, S., P. M. Daniel, and D. Whitteridge. Muscle spindles and other sensory endings in the extrinsic eye muscles; the physiology and anatomy of these receptors and of their connections with the brain stem. Brain 78: 564–583, 1955.
 73. Crommelinck, M., D. Guitton, and A. Roucoux. Retino‐topic versus spatial coding of saccades: clues obtained by stimulating deep layers of cat's superior colliculus. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, p. 425–435.
 74. Crommelinck, M., and A. Roucoux. Characteristics of cat's eye saccades in different states of alertness. Brain Res. 103: 574–578, 1976.
 75. Dallos, P. J., and R. W. Jones. Learning behavior of the eye fixation control system. IEEE Trans. Autom. Control AC‐8: 218–227, 1963.
 76. Daroff, R. B., and W. F. Hoyt. Supranuclear disorders of ocular control systems in man. Clinical, anatomical and physiological correlations. In: Control of Eye Movements, edited by P. Bach‐y‐Rita and C. C. Collins. New York: Academic, 1971, p. 175–235.
 77. Delgado‐Garcia, J., R. Baker, and S. M. Highstein. The activity of internuclear neurons identified within the abducens nucleus of the alert cat. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, p. 291–300.
 78. Dichgans, J., and R. Jung. Oculomotor abnormalities due to cerebellar lesions. In: Basic Mechanisms of Ocular Motility and Their Clinical Implications, edited by G. Lennerstrand and P. Bach‐y‐Rita. Oxford: Pergamon, 1975, vol. 24, p. 281–298. (Wenner‐Gren Cent. Int. Symp. Ser.).
 79. Dichgans, J., C. L. Schmidt, and W. Graf. Visual input improves the speedometer function of the vestibular nuclei in the goldfish. Exp. Brain Res. 18: 319–322, 1973.
 80. Ditchburn, R. W. Eye‐Movements and Visual Perception. Oxford: Clarendon, 1973.
 81. Dodge, R., and T. S. Cline. The angle velocity of eye movements. Psychol. Rev. 8: 145–157, 1901.
 82. Dubois, M. F. W., and H. Collewijn. The optokinetic reactions of the rabbit: relation to the visual streak. Vision Res. 19: 9–17, 1979.
 83. Easter, S. S., Jr. Spontaneous eye movements in restrained goldfish. Vision Res. 11: 333–342, 1971.
 84. Easter, S. S., Jr. A comment on the glissade. Vision Res. 13: 881–882, 1973.
 85. Easter, S. S., Jr. The time course of saccadic eye movements in goldfish. Vision Res. 15: 405–409, 1975.
 86. Easter, S. S., Jr. P. R. Johns, and D. R. Hechenlively. Horizontal compensatory eye movements in goldfish (Carassius auratus). I. The normal animal. J. Comp. Physiol. 92: 23–35, 1974.
 87. Eckmiller, R. Hysteresis in the static characteristics of eye position coded neurons in the alert monkey. Pfluegers Arch. 350: 249–258, 1974.
 88. Eckmiller, R., and M. Mackeben. Velocity coded neurons: a new class of pre‐motor neurons in the primate oculomotor system during pursuit. Soc. Neurosci. Abstr. 4: 162, 1978.
 89. Estes, M. S., R. H. I. Blanks, and C. H. Markham. Physiological characteristics of vestibular first‐order canal neurons in the cat. I. Response plane determination and resting discharge characteristics. J. Neurophysiol. 38: 1232–1249, 1975.
 90. Evinger, C., and A. F. Fuchs. Saccadic, smooth pursuit, and optokinetic eye movements of the trained cat. J. Physiol. London 285: 209–229, 1978.
 91. Evinger, L. C., A. F. Fuchs, and R. Baker. Bilateral lesions of the medial longitudinal fasciculus in monkeys: effects on the horizontal and vertical components of voluntary and vestibular induced eye movements. Exp. Brain Res. 28: 1–20, 1977.
 92. Evinger, C., C. R. S. Kaneko, G. W. Johanson, and A. F. Fuchs. Omnipauser cells in the cat. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, p. 337–340.
 93. Fender, D. H., and P. W. Nye. An investigation of the mechanisms of eye movement control. Kybernetik 1: 81–88, 1961.
 94. Fernandez, C., and J. M. Goldberg. Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. II. Response to sinusoidal stimulation and dynamics of peripheral vestibular system. J. Neurophysiol. 34: 661–675, 1971.
 95. Fernandez, C., J. M. Goldberg, and W. K. Abend. Response to static tilts of peripheral neurons innervating otolith organs of the squirrel monkey. J. Neurophysiol. 35: 978–997, 1972.
 96. Ferrier, D. The localization of function in brain. Proc. R. Soc. 22: 229–232, 1874.
 97. Fillenz, M. Responses in the brain stem of the cat to stretch of extrinsic ocular muscles. J. Physiol. London 128: 182–199, 1955.
 98. Findlay, J. M. The magnitude of translational head movements. Opt. Acta 16: 65–68, 1969.
 99. Fuchs, A. F. Saccadic and smooth pursuit eye movements in the monkey. J. Physiol. London 191: 609–631, 1967.
 100. Fuchs, A. F., and J. Kimm. Unit activity in vestibular nucleus of the alert monkey during horizontal angular acceleration and eye movement. J. Neurophysiol. 38: 1140–1161, 1975.
 101. Fuchs, A. F., and H. H. Kornhuber. Extraocular muscle afferents to the cerebellum of the cat. J. Physiol. London 200: 713–722, 1969.
 102. Fuchs, A. F., and E. S. Luschei. Firing patterns of abducens neurons of alert monkeys in relationship to horizontal eye movement. J. Neurophysiol. 33: 382–392, 1970.
 103. Fuchs, A. F., and E. S. Luschei. Unit activity in the brainstem related to eye movements. In: Cerebral Control of Eye Movements and Motion Perception, edited by J. Dichgans and E. Bizzi. Basel: Karger, 1972, p. 17–27. (Int. Congr. Physiol. Sci., 25th, Freiberg, July 1971.).
 104. Fuchs, A. F., and D. A. Robinson. A method for measuring horizontal and vertical eye movement chronically in the monkey. J. Appl. Physiol. 21: 1068–1070, 1966.
 105. Furuya, N., K. Kawano, and H. Shimazu. Functional organization of vestibulofastigial projection in the horizontal semicircular canal system in the cat. Exp. Brain Res. 24: 75–87, 1975.
 106. Gacek, R. R. Anatomical demonstration of the vestibuloocular projections in the cat. Laryngoscope 81: 1559–1595, 1971.
 107. Gardner, E. P., and A. F. Fuchs. Single‐unit responses to natural vestibular stimuli and eye movements in deep cerebellar nuclei of the alert rhesus monkey. J. Neurophysiol. 38: 627–649, 1975.
 108. Gauthier, G. M., and J.‐M. Hofferer. Eye tracking of self‐moved targets in the absence of vision. Exp. Brain Res. 26: 121–139, 1976.
 109. Gauthier, G. M., and D. A. Robinson. Adaptation of the human vestibuloocular reflex to magnifying lenses. Brain Res. 92: 331–335, 1975.
 110. Gernant, B. E. Interactions between extraocular myotatic and ascending vestibular activities. Exp. Neurol. 20: 120–134, 1968.
 111. Ghelarducci, B., S. M. Highstein, and M. Ito. Origin of the preoculomotor projections through the brachium conjunctivum and their functional roles in the vestibulo‐ocular reflex. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, p. 167–175.
 112. Ghelarducci, B., M. Ito, and N. Yagi. Impulse discharges from flocculus Purkinje cells of alert rabbits during visual stimulation combined with horizontal head rotation. Brain Res. 87: 66–72, 1975.
 113. Gilbert, P. F. C., and W. T. Thach. Purkinje cell activity during motor learning. Brain Res. 128: 309–328, 1977.
 114. Van Gisbergen, J. A. M., and D. A. Robinson. Generation of micro‐ and macrosaccades by burst neurons in the monkey. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, p. 301–308.
 115. Goebel, H. H., A. Komatsuzaki, M. B. Bender, and B. Cohen. Lesions of the pontine tegmentum and conjugate gaze paralysis. Arch. Neurol. Chicago 24: 431–440, 1971.
 116. Goldberg, J. M., and C. Fernandez. Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. I. Resting discharge and response to constant angular accelerations. J. Neurophysiol. 34: 635–660, 1971.
 117. Goldberg, J. M., and C. Fernandez. Vestibular system. In: Handbook of Physiology. The Nervous System, edited by J. M. Brookhart and V. B. Mountcastle. Bethesda, MD: Am. Physiol. Soc., sect. 1, vol. III. In press.
 118. Goldberg, M. E., and M. C. Bushnell. Monkey frontal eye fields have a neuronal signal that precedes visually guided saccades. Soc. Neurosci. Abstr. 5: 779, 1979.
 119. Gonshor, A., and G. Melvill Jones. Extreme vestibuloocular adaptation induced by prolonged optical reversal of vision. J. Physiol. London 256: 381–414, 1976.
 120. Gonshor, A., and G. Melvill Jones. Short‐term adaptive changes in the human vestibulo‐ocular reflex arc. J. Physiol. London 256: 361–379, 1976.
 121. Grantyn, A., R. Grantyn, and K.‐P. Robiné. Neuronal organization of the tecto‐oculomotor pathways. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, p. 197–206.
 122. Graybiel, A. M. Direct and indirect preoculomotor pathways of the brainstem: an autoradiographic study of the pontine reticular formation in the cat. J. Comp. Neurol. 175: 37–78, 1977.
 123. Graybiel, A. M., and E. A. Hartwieg. Some afferent connections of the oculomotor complex in the cat: an experimental study with tracer techniques. Brain Res. 81: 543–551, 1974.
 124. Green, A. E., and J. Wallman. Rapid change in gain of vestibulo‐ocular reflex in chickens. Soc. Neurosci. Abstr. 4: 163, 1978.
 125. Haddad, G. M., J. L. Demer, and D. A. Robinson. The effect of lesions of the dorsal cap of the inferior olive on the vestibuloocular and optokinetic systems of the cat. Brain Res. 185: 265–275, 1980.
 126. Haddad, G. M., A. R. Friendlich, and D. A. Robinson. Compensation of nystagmus after VIIIth nerve lesions in vestibulocerebellectomized cats. Brain Res. 135: 192–196, 1977.
 127. Haddad, G. M., and D. A. Robinson. Cancellation of the vestibuloocular reflex during active and passive head movements in the normal cat. Soc. Neurosci. Abstr. 3: 155, 1977.
 128. Haddad, G. M., and R. M. Steinman. The smallest voluntary saccade: implications for fixation. Vision Res. 13: 1075–1086, 1973.
 129. Hallett, P. E., and A. D. Lightstone. Saccadic eye movements towards stimuli triggered by prior saccades. Vision Res. 16: 99–106, 1976.
 130. Henn, V., and B. Cohen. Quantitative analysis of activity in eye muscle motoneurons during saccadic eye movements and positions of fixation. J. Neurophysiol. 36: 115–126, 1973.
 131. Henn, V., L. R. Young, and C. Finley. Vestibular nucleus units in alert monkeys are also influenced by moving visual fields. Brain Res. 71: 144–149, 1974.
 132. Henson, D. B. Corrective saccades: effects of altering visual feedback. Vision Res. 18: 63–67, 1978.
 133. Henson, D. B. Investigation into corrective saccadic eye movements for refixation amplitudes of 10 degrees and below. Vision Res. 19: 57–61, 1979.
 134. Heywood, S., and G. Ratcliff. Long‐term oculomotor consequences of unilateral colliculectomy in man. In: Basic Mechanisms of Ocular Motility and Their Clinical Implications, edited by G. Lennerstrand and P. Bach‐y‐Rita. Oxford: Pergamon, 1975, vol. 24, p. 561–564. (Wenner‐Gren Cent. Int. Symp. Ser.).
 135. Highstein, S. M., and R. Baker. Excitatory termination of abducens internuclear neurons on medial rectus motoneurons: relationship to syndrome of internuclear ophthalmoplegia. J. Neurophysiol. 41: 1647–1661, 1978.
 136. Hikosaka, O., Y. Igusa, S. Nakao, and H. Shimazu. Direct inhibitory synaptic linkage of ponto‐medullary reticular burst neurons with abducens motoneurons in the cat. Exp. Brain Res. 33: 337–352, 1978.
 137. Hikosaka, O., and T. Kawakami. Inhibitory reticular neurons related to the quick phase of vestibular nystagmus—their location and projection. Exp. Brain Res. 27: 377–396, 1977.
 138. Hikosaka, O., M. Maeda, S. Nakao, H. Shimazu, and Y. Shinoda. Presynaptic impulses in the abducens nucleus and their relation to postsynaptic potentials in motoneurons during vestibular nystagmus. Exp. Brain Res. 27: 355–376, 1977.
 139. Van der Hoeve, J. and A. De Kleijn. Tonische labyrinth Reflexe auf die Augen. Pfluegers Arch. Gesamte Physiol. Menschen Tiere 169: 241–262, 1917.
 140. Hoffmann, K.‐P., and A. Schoppmann. Retinal input to direction selective cells in the nucleus tractus opticus of the cat. Brain Res. 99: 359–366, 1975.
 141. Hughes, A. Topographical relationships between the anatomy and physiology of the rabbit visual system. Doc. Ophthalmol. 30: 33–159, 1971.
 142. Hyde, J. E. Some characteristics of voluntary human ocular movements in the horizontal plane. Am. J. Ophthalmol. 48: 85–94, 1959.
 143. Ito, M. Neural design of the cerebellar motor control system. Brain Res. 40: 81–84, 1972.
 144. Ito, M., Functional specialization of flocculus Purkinje cells and their differential localization determined in connection with the vestibuloocular reflex. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, p. 177–186.
 145. Ito, M., and Y. Miyashita. The effects of chronic destruction of the inferior olive upon visual modification of the horizontal vestibuloocular reflex of rabbits. Proc. Jpn. Acad. 51: 716–720, 1975.
 146. Ito, M., T. Shiida, N. Yagi, and M. Yamamoto. The cerebellar modification of rabbit's horizontal vestibulo‐ocular reflex induced by sustained head rotation combined with visual stimulation. Proc. Jpn. Acad. 50: 85–89, 1974.
 147. Ito, M., T. Shiida, N. Yagi, and M. Yamamoto. Visual influence on rabbit horizontal vestibulo‐ocular reflex presumably effected via the cerebellar flocculus. Brain Res. 65: 170–174, 1974.
 148. Jampel, R. S. Representation of the near response on the cerebral cortex of the macaque. Am. J. Ophthalmol. 48: 573–582, 1959.
 149. J. C. Living without a balancing mechanism. N. Eng. J. Med. 246: 458–460, 1952.
 150. Joyce, G. C., and P. M. H. Rack. Isotonic lengthening and shortening movements of cat soleus muscle. J. Physiol. London 204: 475–491, 1969.
 151. Judge, S. J., B. J. Richmond, and F. C. Chu. Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res. 20: 535–538, 1980.
 152. Jürgens, R., W. Becker, and P. Rieger. The programming of fast eye movements during natural vestibular stimulation—two types of interaction. IFAC Symp. Control Mech. Bio‐Ecosystems, Leipzig, Sept. 12–16, 1977, vol. 3, p. 120–129.
 153. Kaneko, C. R. S., and A. F. Fuchs. Connections of feline omnipause neurons. Soc. Neurosci. Abstr. 4: 164, 1978.
 154. Keller, E. L. Accommodative vergence in the alert monkey. Vision Res. 13: 1565–1575, 1973.
 155. Keller, E. L. Participation of medial pontine reticular formation in eye movement generation in monkey. J. Neurophysiol. 37: 316–332, 1974.
 156. Keller, E. L. Gain of the vestibulo‐ocular reflex in monkey at high rotational frequencies. Vision Res. 18: 311–315, 1978.
 157. Keller, E. L., and P. D. Daniels. Oculomotor related interaction of vestibular and visual stimulation in vestibular nucleus cells in alert monkey. Exp. Neurol. 46: 187–198, 1975.
 158. Keller, E. L., and B. Y. Kamath. Characteristics of head rotation and eye movement related neurons in alert monkey vestibular nucleus. Brain Res. 100: 182–187, 1975.
 159. Keller, E. L., and W. Precht. Persistence of visual responses in vestibular nucleus neurons in cerebellectomized cat. Exp. Brain. Res. 32: 591–594, 1978.
 160. Keller, E. L., and D. A. Robinson. Absence of a stretch reflex in extraocular muscles of the monkey. J. Neurophysiol. 34: 908–919, 1971.
 161. Keller, E. L., and D. A. Robinson. Abducens unit behavior in the monkey during vergence movements. Vision Res. 12: 369–382, 1972.
 162. King, W. M., and A. F. Fuchs. Reticular control of vertical saccadic eye movements by mesencephalic burst neurons. J. Neurophysiol. 42: 861–876, 1979.
 163. King, W. M., A. F. Fuchs, and M. Magnin. Vertical eye movement‐related responses of neurons in midbrain near interstitial nucleus of Cajal. J. Neurophysiol. 46: 549–562, 1981.
 164. King, W. M., S. G. Lisberger, and A. F. Fuchs. Responses of fibers in medial longitudinal fasciculus (MLF) of alert monkeys during horizontal and vertical conjugate eye movements evoked by vestibular or visual stimuli. J. Neurophysiol. 39: 1135–1149, 1976.
 165. Koerner, F., and P. H. Schiller. The optokinetic response under open and closed loop conditions in the monkey. Exp. Brain Res. 14: 318–330, 1972.
 166. Kommerell, G., and U. Klein. Über die visuelle Regelung der Okulomotorik: die optomotorische Wirkung exzentrischer Nachbilder. Vision Res. 11: 905–920, 1971.
 167. Kommerell, G., D. Olivier, and H. Theopold. Adaptive programming of phasic and tonic components in saccadic eye movements. Investigations in patients with abducens palsy. Invest. Ophthalmol. 15: 657–660, 1976.
 168. Körner, F. H., Non‐visual control of human saccadic eye movements. In: Basic Mechanisms of Ocular Motility and Their Clinical Implications, edited by G. Lennerstrand and P. Bach‐y‐Rita. Oxford: Pergamon, 1975, vol. 24, p. 565–569. (Wenner‐Gren Cent. Int. Symp. Ser.).
 169. Kowler, E., B. J. Murphy, and R. M. Steinman. Velocity matching during smooth pursuit of different targets on different backgrounds. Vision Res. 18: 603–605, 1978.
 170. Kris, C. Corneo‐fundal potential variations during light and dark adaptation. Nature London 182: 1027–1028, 1958.
 171. Landers, P. H., and A. Taylor. Transfer function analysis of the vestibulo‐ocular reflex in the conscious cat. In: Basic Mechanisms of Ocular Motility and Their Clinical Implications, edited by G. Lennerstrand and P. Bach‐y‐Rita. Oxford: Pergamon, 1975, vol. 24, p. 505–508. (Wenner‐Gren Cent. Int. Symp. Ser.).
 172. Lange, B. In wieweit sind die Symptome, welche nach Zerstörung des Kleinhirns beobachtet werden, auf Verletzungen des Acusticus zurückzuführen? Pfluegers Arch. Gesamte Physiol. Menschen Tiere 50: 612–625, 1891.
 173. Latto, R., and A. Cowey. Frontal eye‐field lesions in monkeys. In: Cerebral Control of Eye Movements and Motion Perception, edited by J. Dichgans and E. Bizzi. Basel: Karger, 1972, p. 159–168. (Int. Congr. Physiol. Sci., 25th, Freiberg, July, 1971.).
 174. Lennerstrand, G., Motor units in eye muscles. In: Basic Mechanisms of Ocular Motility and Their Clinical Implications, edited by G. Lennerstrand and P. Bach‐y‐Rita. Oxford: Pergamon, 1975, vol. 24, p. 119–143. (Wenner‐Gren Cent. Int. Symp. Ser.).
 175. Lisberger, S. G., L. C. Evinger, and G. W. Johanson. Smooth pursuit tracking of periodic and non‐periodic targets in man. Soc. Neurosci. Abstr. 3: 156, 1977.
 176. Lisberger, S. G., and A. F. Fuchs. Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. I. Purkinje cell activity during visually guided horizontal smooth‐pursuit eye movements and passive head rotation. J. Neurophysiol. 41: 733–763, 1978.
 177. Lisberger, S. G., and A. F. Fuchs. Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. II. Mossy fiber firing patterns during horizontal head rotation and eye movement. J. Neurophysiol. 41: 764–777, 1978.
 178. Llinás, R., and K. Walton. Significance of the olivo‐cerebellar system in compensation of ocular position following unilateral labyrinthectomy. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, p. 399–408.
 179. Llinás, R., K. Walton, D. E. Hillman, and C. Sotelo. Inferior olive: its role in motor learning. Science 190: 1230–1231, 1975.
 180. Llinás, R., and J. W. Wolfe. Functional linkage between the electrical activity in the vermal cerebellar cortex and saccadic eye movements. Exp. Brain Res. 29: 1–14, 1977.
 181. Lorente de Nó, R. Vestibulo‐ocular reflex arc. Arch. Neurol. Psychiatry 30: 245–291, 1933.
 182. Luschei, E. S., and A. F. Fuchs. Activity of brain stem neurons during eye movements of alert monkeys. J. Neurophysiol. 35: 445–461, 1972.
 183. Lynch, J. C., V. B. Mountcastle, W. H. Talbot, and T. C. T. Yin. Parietal lobe mechanisms for directed visual attention. J. Neurophysiol. 40: 362–389, 1977.
 184. Maciewicz, R. J., and R. F. Spencer. Oculomotor and abducens internuclear pathways in the cat. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, p. 99–108.
 185. Maekawa, K., and T. Takeda. Afferent pathways from the visual system to the cerebellar flocculus of the rabbit. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, p. 187–195.
 186. Maffei, L., and A. Fiorentini. Oculomotor proprioception in the cat. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977. p. 477–481.
 187. Malcolm, R., and G. Melvill Jones. A quantitative study of vestibular adaptation in humans. Acta Oto‐Laryngol. 70: 126–135, 1970.
 188. Manni, E., R. Bortolami, and C. Desole. Peripheral pathway of eye muscle proprioception. Exp. Neurol. 22: 1–12, 1968.
 189. Manni, E., G. Palmieri, and R. Marini. Central pathway of the extraocular muscle proprioception. Exp. Neurol. 42: 181–190, 1974.
 190. Marr, D. A theory of cerebellar cortex. J. Physiol. London 202: 437–470, 1969.
 191. McCabe, B. F., and J. H. Ryu. Further experiments on vestibular compensation. Laryngoscope 82: 381–396, 1972.
 192. Meiry, J. L., Vestibular and proprioceptive stabilization of eye movements. In: Control of Eye Movements, edited by P. Bach‐y‐Rita and C. C. Collins. New York: Academic, 1971, p. 483–496.
 193. Melvill Jones, G. Predominance of anticompensatory oculomotor response during rapid head rotation. Aerosp. Med. 35: 965–968, 1964.
 194. Melvill Jones, G. Interactions between optokinetic and vestibulo‐ocular responses during head rotation in various planes. Aerosp. Med. 37: 172–177, 1966.
 195. Melvill Jones, G., and P. Davies. Adaptation of cat vestibulo‐ocular reflex to 200 days of optically reversed vision. Brain Res. 103: 551–554, 1976.
 196. Melvill Jones, G., and J. H. Milsum. Frequency‐response analysis of central vestibular unit activity resulting from rotational stimulation of the semicircular canals. J. Physiol. London 219: 191–215, 1971.
 197. Melvill Jones, G., and K. E. Spells. A theoretical and comparative study of the functional dependence of the semicircular canal upon its physical dimensions. Proc. R. Soc. London Ser. B 157: 403–419, 1963.
 198. Michael, J., and G. Melvill Jones. Dependence of visual tracking capability upon stimulus predictability. Vision Res. 6: 707–716, 1966.
 199. Miles, F. A. Single unit firing patterns in the vestibular nuclei related to voluntary eye movements and passive body rotation in conscious monkeys. Brain Res. 71: 215–224, 1974.
 200. Miles, F. A., The primate flocculus and eye‐head coordination. In: Eye Movements, edited by B. A. Brooks and F. J. Bajandas. New York: Plenum, 1977, p. 45–92. (ARVO Symp., 1976.).
 201. Miles, F. A., and J. H. Fuller. Adaptive plasticity in the vestibuloocular responses of the rhesus monkey. Brain Res. 80: 512–516, 1974.
 202. Miles, F. A., and J. H. Fuller. Visual tracking and the primate flocculus. Science 189: 1000–1002, 1975.
 203. Miller, E. F. Counter‐rolling of the human eyes produced by head tilt with respect to gravity. Acta Oto‐Laryngol. 54: 479–501, 1962.
 204. Mohler, C. W., and R. H. Wurtz. Organization of monkey superior colliculus: intermediate layer cells discharging before eye movements. J. Neurophysiol. 39: 722–744, 1976.
 205. Mohler, C. W., and R. H. Wurtz. Role of striate cortex and superior colliculus in visual guidance of saccadic eye movements in monkeys. J. Neurophysiol. 40: 74–94, 1977.
 206. Morasso, P., E. Bizzi, and J. Dichgans. Adjustment of saccadic characteristics during head movements. Exp. Brain Res. 16: 492–500, 1973.
 207. Murphy, B. J., E. Kowler, and R. M. Steinman. Slow oculomotor control in the presence of moving backgrounds. Vision Res. 15: 1263–1268, 1975.
 208. Noda, H., R. Asoh, and M. Shibagaki. Floccular unit activity associated with eye movements and fixation. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, p. 371–380.
 209. O'Leary, D. P., and V. Honrubia. Analysis of afferent response from isolated semicircular canal of the guitarfish using rotational acceleration white‐noise inputs. II. Estimation of linear system parameters and gain and phase spectra. J. Neurophysiol. 39: 645–659, 1976.
 210. Ono, H., S. Nakamizo, and M. J. Steinbach. Nonadditivity of vergence and saccadic eye movements. Vision Res. 18: 735–739, 1978.
 211. Optican, L. M., and D. A. Robinson. Cerebellar‐dependent adaptive control of the primate saccadic system. J. Neurophysiol. 44: 1058–1076, 1980.
 212. Oyster, C. W., E. Takahashi, and H. Collewijn. Direction‐selective retinal ganglion cells and control of optokinetic nystagmus in the rabbit. Vision Res. 12: 183–193, 1972.
 213. Perlmutter, A. L., and A. E. Kertesz. Measurement of human vertical fusional response. Vision Res. 18: 219–223, 1978.
 214. Poggio, G. F., R. W. Doty, Jr. and W. H. Talbot. Foveal striate cortex of behaving monkey: single‐neuron responses to square‐wave gratings during fixation of gaze. J. Neurophysiol. 40: 1369–1391, 1977.
 215. Pola, J., and D. A. Robinson. Oculomotor signals in medial longitudinal fasciculus of the monkey. J. Neurophysiol. 41: 245–259, 1978.
 216. Pola, J. R., and H. J. Wyatt. Smooth pursuit eye movements to stationary targets (Abstract). Proc. Assoc. Res. Vision Ophthalmol., Sarasota, April 30‐May 4, 1979, p. 103.
 217. Prablanc, C., and M. Jeannerod. Corrective saccades: dependence on retinal reafferent signals. Vision Res. 15: 465–469, 1975.
 218. Precht, W., The functional synaptology of brainstem oculomotor pathways. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, p. 131–141.
 219. Precht, W., and P. Strata. On the pathways mediating optokinetic responses in vestibular nuclear neurons. Neuroscience 5: 777–787, 1980.
 220. Rademaker, G. G. J., and J. W. G. ter Braak. On the central mechanism of some optic reactions. Brain 71: 48–76, 1948.
 221. Raphan, T., V. Matsuo, and B. Cohen. Velocity storage in the vestibuloocular reflex arc (VOR). Exp. Brain Res. 35: 229–248, 1979.
 222. Rashbass, C., and G. Westheimer. Disjunctive eye movements. J. Physiol. London 159: 339–360, 1961.
 223. Raybourn, M. S., and E. L. Keller. Colliculoreticular organization in primate oculomotor system. J. Neurophysiol. 40: 861–878, 1977.
 224. Riggs, L. A., and E. W. Niehl. Eye movements recorded during convergence and divergence. J. Opt. Soc. Am. 50: 913–920, 1960.
 225. Ritchie, L. Effects of cerebellar lesions in saccadic eye movements. J. Neurophysiol. 39: 1246–1256, 1976.
 226. Robinson, D. A. A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Trans. Bio‐Med. Electron. BME‐10; 137–145, 1963.
 227. Robinson, D. A. The mechanics of human saccadic eye movement. J. Physiol. London 174: 245–264, 1964.
 228. Robinson, D. A. The mechanics of human smooth pursuit eye movement. J. Physiol. London 180: 569–591, 1965.
 229. Robinson, D. A. Oculomotor unit behavior in the monkey. J. Neurophysiol. 33: 393–404, 1970.
 230. Robinson, D. A. Eye movements evoked by collicular stimulation in the alert monkey. Vision Res. 12: 1795–1808, 1972.
 231. Robinson, D. A. Models of the saccadic eye movement control system. Kybernetik 14: 71–83, 1973.
 232. Robinson, D. A. The effect of cerebellectomy on the cat's vestibuloocular integrator. Brain Res. 71: 195–207, 1974.
 233. Robinson, D. A., Oculomotor control signals. In: Basic Mechanisms of Ocular Motility and Their Clinical Implications, edited by P. Bach‐y‐Rita and G. Lennerstrand. Oxford: Pergamon, 1975, vol. 24, p. 337–374. (Wenner‐Gren Cent. Int. Symp. Ser.).
 234. Robinson, D. A. A quantitative analysis of extraocular muscle cooperation and squint. Invest. Ophthalmol. 14: 801–825, 1975.
 235. Robinson, D. A. Adaptive gain control of vestibuloocular reflex by the cerebellum. J. Neurophysiol. 39: 954–969, 1976.
 236. Robinson, D. A. Linear addition of optokinetic and vestibular signals in the vestibular nucleus. Exp. Brain Res. 30: 447–450, 1977.
 237. Robinson, D. A., The functional behavior of the peripheral oculomotor apparatus: a review. In: Disorders of Ocular Motility, edited by G. Kommerell. München: Bergmann, 1978, p. 43–61.
 238. Robinson, D. A., and A. F. Fuchs. Eye movements evoked by stimulation of the frontal eye fields. J. Neurophysiol. 32: 637–648, 1969.
 239. Robinson, D. A., and E. L. Keller. The behavior of eye movement motoneurons in the alert monkey. Bibl. Ophthalmol. 82: 7–16, 1972.
 240. Robinson, D. A, D. M. O'Meara, A. B. Scott, and C. C. Collins. Mechanical components of human eye movements. J. Appl. Physiol. 26: 548–553, 1969.
 241. Robinson, D. L., M. E. Goldberg, and G. B. Stanton. Parietal association cortex in the primate: sensory mechanisms and behavioral modulations. J. Neurophysiol. 41: 910–932, 1978.
 242. Ron, S., and D. A. Robinson. Eye movements evoked by cerebellar stimulation in the alert monkey. J. Neurophysiol. 36: 1004–1022, 1973.
 243. Ron, S., D. A. Robinson, and A. A. Skavenski. Saccades and the quick phases of nystagmus. Vision Res. 12: 2015–2022, 1972.
 244. Russo, J. E., Adaptation of cognitive processes to the eye movement system. In: Eye Movements and the Higher Psychological Functions, edited by J. W. Senders, D. F. Fisher, and R. A. Monty. Hillsdale, NJ: Erlbaum, 1978, p. 89–112.
 245. Schaefer, K.‐P., and D. L. Meyer. Compensatory mechanisms following labyrinthine lesions in the guinea‐pig. A simple model of learning. In: Memory and Transfer of Information, edited by H. P. Zippel. New York: Plenum, 1973, p. 203–232.
 246. Schaefer, K.‐P., and D. L. Meyer. Compensation of vestibular lesions. In: Handbook of Sensory Physiology. Vestibular System, edited by H. H. Kornhuber. Berlin: Springer‐Verlag, 1974, vol. VI, pt. 1, p. 463–490.
 247. Schairer, J. O., and M. V. L. Bennett. Adaptive gain control in vestibuloocular reflex of goldfish. Soc. Neurosci. Abstr. 3: 157, 1977.
 248. Schiller, P. H. The discharge characteristics of single units in the oculomotor and abducens nuclei of the unanesthetized monkey. Exp. Brain Res. 10: 347–362, 1970.
 249. Schiller, P. H., and M. Stryker. Single‐unit recording and stimulation in superior colliculus of the alert rhesus monkey. J. Neurophysiol. 35: 915–924, 1972.
 250. Schiller, P. H., S. D. True, and J. L. Conway. Effects of frontal eye field and superior colliculus ablations on eye movements. Science 206: 590–592, 1979.
 251. Schlag, J., and M. Schlag‐Rey. Visuomotor properties of cells in cat thalamic internal medullary lamina. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, p. 453–462.
 252. Shebilske, W. L., Visuomotor coordination in visual direction and position constancies. In: Stability and Constancy in Visual Perception: Mechanisms and Processes, edited by W. Epstein. New York: Wiley, 1977, p. 23–69.
 253. Shimazu, H., and W. Precht. Inhibition of central vestibular neurons from the contralateral labyrinth and its mediating pathway. J. Neurophysiol. 29: 467–492, 1966.
 254. Shimazu, H., and C. M. Smith. Cerebellar and labyrinthine influences on single vestibular neurons identified by natural stimuli. J. Neurophysiol. 34: 493–508, 1971.
 255. Shults, W. T., L. Stark, W. F. Hoyt, and A. L. Ochs. Normal saccadic structure of voluntary nystagmus. Arch. Ophthalmol. 95: 1399–1404, 1977.
 256. Simpson, J. I., and R. Hess. Complex and simple visual messages in the flocculus. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, p. 351–360.
 257. Sindermann, F., B. Geiselmann, and M. Fischler. Single motor unit activity in extraocular muscles in man during fixation and saccades. Electroencephalogr. Clin. Neurophysiol. 45: 64–73, 1978.
 258. Skavenski, A. A., G. Haddad, and R. M. Steinman. The extraretinal signal for the visual perception of direction. Percept. Psychophys. 11: 287–290, 1972.
 259. Skavenski, A. A., and R. M. Hansen. Role of eye position information in visual space perception. In: Eye Movements and the Higher Psychological Functions, edited by J. W. Senders, D. F. Fisher, and R. A. Monty. Hillsdale, NJ: Erlbaum, 1978, p. 15–34.
 260. Skavenski, A. A., R. M. Hansen, R. M. Steinman, and B. J. Winterson. Quality of retinal image stabilization during small natural and artificial body rotations in man. Vision Res. 19: 675–683, 1979.
 261. Skavenski, A. A., and D. A. Robinson. Role of abducens neurons in vestibuloocular reflex. J. Neurophysiol. 36: 724–738, 1973.
 262. Skavenski, A. A., D. A. Robinson, R. M. Steinman, and G. T. Timberlake. Miniature eye movements of fixation in rhesus monkey. Vision Res. 15: 1269–1273, 1975.
 263. Sparks, D. L., and J. G. Pollack. The neural control of saccadic eye movements: the role of the superior colliculus. In: Eye Movements, edited by B. A. Brooks and F. J. Bajandas. New York: Plenum, 1977, p. 179–219. (ARVO Symp., 1976.).
 264. Stark, L., G. Vossius, and L. R. Young. Predictive control of eye tracking movements. Trans. Inst. Radio Eng. Prof. Group Hum. Factors Electron. HFE‐3: 52–56, 1962.
 265. St Cyr, G. J., and D. H. Fender. Nonlinearities of the human oculomotor system: gain. Vision Res. 9: 1235–1246, 1969.
 266. Steinbach, M. J. Eye tracking of self‐moved targets: the role of efference. J. Exp. Psychol. 82: 366–376, 1969.
 267. Steinbach, M. J. Pursuing the perceptual rather than the retinal stimulus. Vision Res. 16: 1371–1376, 1976.
 268. Steinhausen, W. Über die Beobachtung der Cupula in den Bogengangsampullen des Labyrinths des Lebenden Hechts, Pfluegers Arch. Gesamte Physiol. Menschen Tiere 232: 500–512, 1933.
 269. Steinman, R. M. Effects of target size, luminance, and color on monocular fixation. J. Opt. Soc. Am. 55: 1158–1165, 1965.
 270. Steinman, R. M., G. M. Haddad, A. A. Skavenski, and D. Wyman. Miniature eye movement. Science 181: 810–819, 1973.
 271. Stone, J., and Y. Fukuda. Properties of cat retinal ganglion cells: a comparison of W‐cells with X‐ and Y‐cells. J. Neurophysiol. 37: 722–748, 1974.
 272. Stryker, M., and C. Blakemore. Saccadic and disjunctive eye movements in cats. Vision Res. 12: 2005–2013, 1972.
 273. Suzuki, J.‐I., B. Cohen, and M. B. Bender. Compensatory eye movements induced by vertical semicircular canal stimulation. Exp. Neurol. 9: 137–160, 1964.
 274. Szentágothai, J. Die zentrale Innervation der Augenbewegungen. Arch. Psychiatr. Nervenkr. 116: 721–760, 1943.
 275. Szentágothai, J. The elementary vestibulo‐ocular reflex arc. J. Neurophysiol. 13: 395–407, 1950.
 276. Takemori, S. The similarities of optokinetic after‐nystagmus to the vestibular nystagmus. Ann. Otol. Rhinol. Laryngol. 83: 230–238, 1974.
 277. Takemori, S., and B. Cohen. Loss of visual suppression of vestibular nystagmus after flocculus lesions. Brain Res. 72: 213–224, 1974.
 278. Tarlov, E., Anatomy of the two vestibulo‐oculomotor projection systems. In: Progress in Brain Research. Basic Aspects of Central Vestibular Mechanisms, edited by A. Brodal and O. Pompeiano. Amsterdam: Elsevier, 1972, vol. 37, p. 471–491.
 279. Troost, B. T., R. B. Daroff, R. B. Weber, and L. F. Dell'Osso. Hemispheric control of eye movements. II. Quantitative analysis of smooth pursuit in a hemispherectomy patient. Arch. Neurol. Chicago. 27: 449–452, 1972.
 280. Uemura, T., and B. Cohen. Vestibulo‐ocular reflexes: effects of vestibular nuclear lesions. In: Progress in Brain Research. Basic Aspects of Central Vestibular Mechanisms, edited by A. Brodal and O. Pompeiano. Amsterdam: Elsevier, 1972, vol. 37, p. 515–528.
 281. Waespe, W., and V. Henn. Behavior of secondary vestibular units during optokinetic nystagmus and after‐nystagmus in alert monkeys. Pfluegers Arch. 362: (Suppl. 197), R50, 1976.
 282. Waespe, W., and V. Henn. Neuronal activity in the vestibular nuclei of the alert monkey during vestibular and optokinetic stimulation. Exp. Brain Res. 27: 523–538, 1977.
 283. Warwick, R., Oculomotor organization. In: Oculomotor System, edited by M. B. Bender. New York: Harper & Row, 1964, p. 173–202.
 284. Weber, R. B., and R. B. Daroff. Corrective movements following refixation saccades: type and control system analysis. Vision Res. 12: 467–475, 1972.
 285. Westheimer, G. Eye movement responses to a horizontally moving visual stimulus. AMA Arch. Ophthalmol. 52: 932–941, 1954.
 286. Westheimer, G. Mechanism of saccadic eye movements. AMA Arch. Ophthalmol. 52: 710–724, 1954.
 287. Westheimer, G., and S. M. Blair. Saccadic inhibition induced by brain‐stem stimulation in the alert monkey. Invest. Ophthalmol. 12: 77–78, 1973.
 288. Westheimer, G., and S. M. Blair. Oculomotor defects in cerebellectomized monkeys. Invest. Ophthalmol. 12: 618–621, 1973.
 289. Westheimer, G., and D. E. Mitchell. The sensory stimulus for disjunctive eye movements. Vision Res. 9: 749–755, 1969.
 290. Wheeless, L. L., Jr. R. M. Boynton, and G. H. Cohen. Eye movement responses to step and pulse‐step stimuli. J. Opt. Soc. Am. 56: 956–960, 1966.
 291. Whitteridge, D. The motor nerve supply to the extra‐ocular muscle spindles (Abstract). Electroencephalogr. Clin. Neurophysiol. 10: 353, 1958.
 292. Whitteridge, D., Central control of eye movements. In: Handbook of Physiology. Neurophysiology, edited by J. Field and H. W. Magoun. Washington, DC: Am. Physiol. Soc., 1960, sect. 1, vol. II, chapt. XLII, p. 1089–1109.
 293. Wilkie, D. R. The mechanical properties of muscle. Br. Med. Bull. 12: 177–182, 1956.
 294. Winterson, B. J., and H. Collewijn. Microsaccades during finely guided visuomotor tasks. Vision Res. 16: 1387–1390, 1976.
 295. Winterson, B. J., and D. A. Robinson. Fixation by the alert but solitary cat. Vision Res. 15: 1349–1352, 1975.
 296. Winterson, B. J., and R. M. Steinman. The effects of luminance of human smooth pursuit of perifoveal and foveal targets. Vision Res. 18: 1165–1172, 1978.
 297. Wurtz, R. H., and M. E. Goldberg. Activity of superior colliculus in behaving monkey. III. Cells discharging before eye movement. J. Neurophysiol. 35: 575–586, 1972.
 298. Wurtz, R. H., and M. E. Goldberg. Activity of superior colliculus in behaving monkey. IV. Effects of lesions on eye movement. J. Neurophysiol. 35: 587–596, 1972.
 299. Yarbus, A. L. Motion of the eye on interchanging fixation points at rest in space. Biophyscis. USSR 2: 679–683, 1957.
 300. Yee, R. D., R. W. Baloh, V. Honrubia, C. G. Y. Lau, and H. A. Jenkins. Slow buildup of optokinetic nystagmus associated with downbeat nystagmus (Abstract). Proc. Assoc. Res. Vision Ophthalmol. Sarasota, April 30–May 4, 1979, p 264.
 301. Young, L. R. The current status of vestibular system models. Automatica 5: 369–383, 1969.
 302. Young, L. R., Pursuit eye tracking movements. In: Control of Eye Movements, edited by P. Bach‐y‐Rita and C. C. Collins. New York: Academic, 1971, p. 429–443.
 303. Young, L. R., and D. Sheena. Survey of eye movement recording methods. Behav. Res. Methods and Instrum. 7: 397–429, 1975.
 304. Young, L. R., and L. Stark. Variable feedback experiments testing a sampled data model for eye tracking movements. IEEE Trans. Prof. Tech. Group Hum. Factors Electron. HFE‐4: 38–51, 1963.
 305. Zee, D. S., Disorders of eye/head coordination. In: Eye Movements, edited by B. A. Brooks and F. J. Bajandas. New York: Plenum, 1977, p. 9–39. (ARVO Symp., 1976.).
 306. Zee, D. S., A. R. Friendlich, and D. A. Robinson. The mechanism of downbeat nystagmus. Arch. Neurol. Chicago 30: 227–237, 1974.
 307. Zee, D. S., L. M. Optican, J. D. Cook, D. A. Robinson, and W. K. Engel. Slow saccades in spinocerebellar degeneration. Arch. Neurol. Chicago 33: 243–251, 176.
 308. Zee, D. S., and D. A. Robinson. Clinical applications of oculomotor models. In: Topics in Neuro‐Ophthalmology, edited by H. S. Thompson. Baltimore: Williams & Wilkins, 1979, p. 266–285.
 309. Zee, D. S., and D. A. Robinson. An hypothetical explanation of saccadic oscillations. Ann. Neurol. 5: 405–414, 1979.
 310. Zee, D. S., and A. Yamazaki, and G. Gücër. Ocular motor abnormalities in trained monkeys with floccular lesions. Soc. Neurosci. Abstr. 4: 168, 1978.
 311. Zee, D. S., R. D. Yee, D. G. Cogan, D. A. Robinson, and W. K. Engel. Oculomotor abnormalities in hereditary cerebellar ataxia. Brain 99: 207–234, 1976.
 312. Zee, D. S., R. D. Yee, and D. A. Robinson. Optokinetic responses in labyrinthine‐defective human beings. Brain Res. 113:423–428, 1976.
 313. Zuber, B. L., Control of vergence eye movements. In: Control of Eye Movements, edited by P. Bach‐y‐Rita and C. C. Collins. New York: Academic, 1971, p. 447–471.

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David A. Robinson. Control of Eye Movements. Compr Physiol 2011, Supplement 2: Handbook of Physiology, The Nervous System, Motor Control: 1275-1320. First published in print 1981. doi: 10.1002/cphy.cp010228