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Control of Eye Movements

David A. Robinson

10.1002/cphy.cp010228

Source: Supplement 2: Handbook of Physiology, The Nervous System, Motor Control

Originally published: 1981

Published online: January 2011

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 201; B from Robinson 235; C from Collewijn 63; D from Winterson and Robinson 295; E, F from Fuchs 99; G from Rashbass and Westheimer 222
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 (a–d) 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.

A–D from Robinson and Keller 239; E, F from Robinson 229
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 70
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. 4C 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 8. 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 5. 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. 115; B from Cohen and Komatsuzaki 54
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. 55; cat from Haddad et al. 125; rabbit from Collewijn 63
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. 16; curve W from Westheimer 286; curve Bg from Boghen et al. 34. Animal data obtained from following sources: curve M (monkey) from Fuchs 99; curve F (goldfish) from Easter 85; curve C (cat) from Crommelinck and Roucoux 74
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 224; C from Clark and Crane 49
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 235
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 211


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 201; B from Robinson 235; C from Collewijn 63; D from Winterson and Robinson 295; E, F from Fuchs 99; G from Rashbass and Westheimer 222


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 (a–d) 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.

A–D from Robinson and Keller 239; E, F from Robinson 229


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 70


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. 4C 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 8. 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 5. 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. 115; B from Cohen and Komatsuzaki 54


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. 55; cat from Haddad et al. 125; rabbit from Collewijn 63


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. 16; curve W from Westheimer 286; curve Bg from Boghen et al. 34. Animal data obtained from following sources: curve M (monkey) from Fuchs 99; curve F (goldfish) from Easter 85; curve C (cat) from Crommelinck and Roucoux 74


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 224; C from Clark and Crane 49


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 235


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 211
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Article Title: Control of Eye Movements
 

How to Cite

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