1Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, Maryland 21287; 2Wills Eye Hospital, Thomas Jefferson University, Philadelphia, Pennsylvania 19107; and 3Department of Neurosurgery, University of Alabama at Birmingham, Birmingham, Alabama 35294
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ABSTRACT |
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Lewis, Richard F., David S. Zee, Herschel P. Goldstein, and Barton L. Guthrie. Proprioceptive and Retinal Afference Modify Postsaccadic Ocular Drift. J. Neurophysiol. 82: 551-563, 1999. Drift of the eyes after saccades produces motion of images on the retina (retinal slip) that degrades visual acuity. In this study, we examined the contributions of proprioceptive and retinal afference to the suppression of postsaccadic drift induced by a unilateral ocular muscle paresis. Eye movements were recorded in three rhesus monkeys with a unilateral weakness of one vertical extraocular muscle before and after proprioceptive deafferentation of the paretic eye. Postsaccadic drift was examined in four visual states: monocular viewing with the normal eye (4-wk period); binocular viewing (2-wk period); binocular viewing with a disparity-reducing prism (2-wk period); and monocular viewing with the paretic eye (2-wk period). The muscle paresis produced vertical postsaccadic drift in the paretic eye, and this drift was suppressed in the binocular viewing condition even when the animals could not fuse. When the animals viewed binocularly with a disparity-reducing prism, the drift in the paretic eye was suppressed in two monkeys (with superior oblique pareses) but generally was enhanced in one animal (with a tenotomy of the inferior rectus). When drift movements were enhanced, they reduced the retinal disparity that was present at the end of the saccade. In the paretic-eye-viewing condition, postsaccadic drift was suppressed in the paretic eye and was induced in the normal eye. After deafferentation in the normal-eye-viewing state, there was a change in the vertical postsaccadic drift of the paretic eye. This change in drift was idiosyncratic and variably affected the amplitude and velocity of the postsaccadic drift movements of the paretic eye. Deafferentation of the paretic eye did not affect the postsaccadic drift of the normal eye nor did it impair visually mediated adaptation of postsaccadic drift. The results demonstrate several new findings concerning the roles of visual and proprioceptive afference in the control of postsaccadic drift: disconjugate adaptation of postsaccadic drift does not require binocular fusion; slow, postsaccadic drift movements that reduce retinal disparity but concurrently increase retinal slip can be induced in the binocular viewing state; postsaccadic drift is modified by proprioception from the extraocular muscles, but these modifications do not serve to minimize retinal slip or to correct errors in saccade amplitude; and visually mediated adaptation of postsaccadic drift does not require proprioceptive afference from the paretic eye.
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INTRODUCTION |
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Optimal vision requires that the eyes be
stationary immediately after saccades, the rapid eye movements used to
redirect gaze. Recordings of activity from ocular motoneurons indicate
that a characteristic pattern of innervation is responsible for
postsaccadic eye stability: the slide, a decaying exponential of
innervation that is thought to compensate for relaxation of the orbital
visco-elastic forces (Collins et al. 1975; Fuchs
and Luschei 1970
), and the step, the tonic innervation that
opposes the elastic recoiling forces of the orbital tissues
(Robinson 1970
). To minimize postsaccadic drift, these
neural signals must be matched correctly to the saccadic pulse, and in
the long-term, they must be adjusted to compensate for the mechanical
changes in the oculomotor plant that occur during growth and aging and
for acute pathological changes, such as extraocular muscle pareses. As
these changes may not affect the two eyes symmetrically, the adaptive
mechanism should be capable of modifying the motor output differently
for each eye (disconjugate adaptation) rather than just
changing the innervation equally for both eyes (conjugate adaptation).
Two afferent signals could indicate the presence of postsaccadic drift
and drive adaptive modification of the slide and step of innervation:
image motion on the retina (retinal slip) and proprioceptive input from
the spindles and tendon organs of the extraocular muscles. Retinal slip
clearly has a prominent effect on conjugate and disconjugate adaptation
of postsaccadic drift. In subjects with unilateral extraocular muscle
palsies, chronic monocular viewing with the paretic eye leads to the
suppression of drift in that eye and to the induction of drift in the
opposite direction in the normal, covered eye ("conjugate"
adaptation) (Abel et al. 1978; Kommerell et al.
1976
; Optican and Robinson 1980
). Chronic
binocular viewing can result in suppression of drift in the paretic eye
without producing drift in the normal eye ("disconjugate"
adaptation) (Viirre et al. 1988
). In these experiments,
the paretic eye drifted after saccades, so both retinal and
proprioceptive afferents potentially could have contributed information
about eye motion to the brain. Modification of the retinal signal
alone, however, was sufficient to adaptively alter postsaccadic drift.
The extraocular muscles of primates contain abundant muscle spindles
and tendon organs (Lukas et al. 1994; Ruskell
1978
), and proprioceptive afferents carry signals that encode
both the position and the velocity of the eyes (Fahy and
Donaldson 1998
). Although we reported that proprioception
contributes to the regulation of the amplitude of the saccadic pulse
and the static ocular alignment in animals with unilateral vertical
muscle pareses (Lewis et al. 1994
), little is known
about the possible role of proprioceptive afference in the control of
eye motion immediately after saccades. A potential role for
proprioception is suggested by the finding that manipulation of
proprioceptive afferents by passively rotating the eye modifies
activity of Purkinje cells in the flocculus (Kimura and Maekawa
1981
; Miyashita 1984
), a region of the
cerebellum that is crucial for the adaptation of postsaccadic drift
(Optican et al. 1986
; Zee et al. 1981
).
In the current study, we have examined the effects of modifying visual
afference and of deafferenting the extraocular muscles on postsaccadic
drift in monkeys with unilateral weakness of a vertical extraocular
muscle. The purpose was to analyze the respective roles of retinal and
proprioceptive afference on the regulation of postsaccadic drift.
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METHODS |
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General experimental procedures
The movements of both eyes were recorded using the magnetic field search coil technique in three juvenile rhesus monkeys with unilateral vertical eye muscle pareses. The output signal of the coil system was filtered at 90 Hz, sampled at 250 Hz, and saved to a digital computer. Coil system resolution was ~0.05°. Targets were presented on a bar that was oriented vertically or horizontally and that was located 1.47 m in front of the animal's head. Light-emitting diodes (LEDs) were spaced at 2.5° intervals along the bar. Eye movements were recorded in total darkness, except for the illuminated LED target.
A vertical and horizontal calibration for the position of each eye was obtained for each recording session by having the animal monocularly fixate a series of LEDs in 2.5° increments, ranging from down 20 to up 20° and from left 20 to right 20°. Vertical saccades then were recorded during monocular viewing with the normal eye for target jumps from 0 to up 10°, up 10° to 0, 0 to down 10°, and down 10° to 0. Horizontal saccades were recorded for target jumps from 0 to right 10°, right 10° to 0, 0 to left 10°, and left 10° to 0. During the saccade paradigm, the animals fixated the LED target for 1.0 s before the target moved to a new position. Thirty sets of vertical saccades and 10 sets of horizontal saccades were recorded during each experimental session, and data were acquired 3 days/wk in each visuoproprioceptive state, beginning 3 days after the state was modified.
Surgical procedures
All surgical procedures were performed under pentobarbital
anesthesia (30 mg/kg iv), and all animal care complied with the Johns
Hopkins Medical School veterinary guidelines. Each animal was implanted
with a head holder and binocular scleral search coils (Judge et
al. 1980). In two animals (SO1 and SO2),
a superior oblique paresis was produced by sectioning the trochlear
nerve intracranially. In the third monkey (IR), the inferior
rectus muscle was weakened by sectioning its tendon.
Proprioceptive inputs from the paretic eye were eliminated at a later
date by sectioning the ophthalmic division of the trigeminal nerve
immediately distal to the Gausserian ganglion (Porter et al.
1983). The ophthalmic division of the trigeminal nerve was identified at surgery anatomically and physiologically (with electrical stimulation, which evoked a blink but no eye movement), and the corneal
reflex was absent throughout the postoperative period. It has been
suggested that a portion of the afferent innervation of the extraocular
muscles travels to the brain stem in the ocular motor nerves
(Gentle and Ruskell 1997
) rather than the trigeminal nerve. Nevertheless the cell bodies of the afferent neurons that innervate the extraocular muscles are located in the trigeminal ganglion (Billig et al. 1997
; Porter
1986
) so that section of the ophthalmic division of the
trigeminal nerve immediately distal to the ganglion would deafferent
the extraocular muscles even if some sensory fibers cross to the ocular
motor nerves proximal to the ganglion.
Experimental protocol
After the vertical muscle paresis was induced, the paretic eye was covered immediately with an opaque patch, and the animals viewed monocularly with the normal eye for 4 wk. For monkeys IR and SO1 (see Table 1), the patch then was removed and the animals were viewed binocularly for 2 wk. A base-down wedge prism, with strength that approximated the size of the vertical misalignment with the normal eye straight ahead, then was placed in front of the paretic eye for 2 wk to promote binocular fusion. For monkey SO2, the opaque patch was replaced with a base-down prism for 2 wk. Monkey SO1 subsequently had its paretic eye covered with an opaque patch for 2 wk to allow deadaptation from the binocular/prism state, and then the patch was switched to the normal eye for 2 wk, forcing it to view monocularly with the paretic eye. At the completion of these experiments, the paretic eye of each animal was covered with the opaque patch for 2 wk. The paretic eye then was deafferented proprioceptively, and the preceding protocol was repeated.
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Data analysis
Data were analyzed off-line with an interactive computer program. The position of each eye was calibrated with a third-order polynomial linearization program to compensate for any nonlinearities in the search coil signal. The amplitude of the saccadic pulse was determined by subtracting the eye position at the end of the pulse (p), defined as the position at which eye velocity first dropped <45°/s, from the eye position at the start of the saccade (the point at which eye velocity 1st exceeded 20°/s). The step position (s) for each eye was determined as the position of the eye when eye velocity returned to a steady value of zero, before the subsequent saccade. The vertical "vergence" angle (V) was defined as the vertical position of the paretic eye minus the vertical position of the normal eye, and the vertical retinal disparity was defined as the vertical retinal error of the paretic eye minus the vertical retinal error of the normal eye.
For drift waveforms that were monophasic (Fig.
1, monkey IR), the amplitude
of the postsaccadic drift was defined as (s-p). For drift waveforms
that had more than one component (Fig. 1, monkey SO1), the
amplitude of each drift component was measured by placing marks at the
inflection points in the drift waveform, defined as the points where
eye velocity changed sign. Because the amplitude of the saccadic pulse
in the paretic eye changed after deafferentation (Lewis et al.
1994) and alterations in pulse size potentially could affect
the amplitude of the postsaccadic drift (Optican and Miles
1985
), each measurement of drift amplitude was normalized by
dividing it by the gain of the preceding pulse for that eye. The pulse
gain was defined as (pulse amplitude)/(target displacement).
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To determine the disconjugacy of the changes in postsaccadic drift induced by the visual and proprioceptive manipulations, the change in the drift of the paretic eye (y axis) was plotted against the change in the drift of the normal eye (x axis; see Fig. 2). If the change in drift was limited to the paretic eye, the points for the four saccade types studied would be located on the y axis; if the change was conjugate (equal in the 2 eyes), the points would fall on the y = x line. The overall nearness of the data points to these two lines is therefore a way to measure the disconjugacy of the change in postsaccadic drift and was calculated for each animal by summing the squared error of the four data points (corresponding to the 4 saccades studied) about the y axis and the y = x line.
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The average velocity of the drift of the paretic eye in the 100-ms
period after the initial, rapid postsaccadic movement (x-p, d-p) was quantified as the mean of the absolute value of the
eye velocity measured every 4 ms during this period. Eye velocity was
calculated by differentiating and filtering the position signal with a
seven-point Gaussian filter. When drift movements could be approximated
by an exponential, a time constant was determined by fitting a single
exponential (a + bet/TC) to
the eye movement trace with the least-squared-error. Statistical analysis was performed with two-way ANOVA and Student's
t-test. Unless otherwise specified, all data presented below
are vertical eye movements recorded during monocular viewing with the
normal eye.
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RESULTS |
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Effect of muscle paresis, normal-eye viewing
As previously reported, the unilateral vertical muscle
paresis produced a vertical misalignment of the eyes that increased with down gaze, and hypometric vertical saccades in the paretic eye
relative to the normal eye (Lewis et al. 1994). The
muscle paresis also resulted in vertical postsaccadic drift in the
paretic eye. The monkey with an inferior rectus tenotomy
(IR) displayed monophasic drift movements (s-p) in the
paretic eye in the direction opposite to that of the antecedent saccade
(Fig. 1, Table 2). The two monkeys with a
paresis of the superior oblique muscle (SO1 and
SO2) had vertical postsaccadic drift movements in the paretic eye that consisted of three components after upward saccades (x-p, d-x, s-d) and two components after downward saccades
(d-p, s-d) (Fig. 1, Table 2). In all three animals, the postsaccadic drift in the normal, viewing eye was small in amplitude and its waveform was monophasic (s-p).
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Visually mediated adaptation before deafferentation
EFFECT OF BINOCULAR VISION WITHOUT A PRISM. When the patch was removed from the paretic eye for monkeys IR and SO1, the animals viewed binocularly but were not able to fuse the images from the two eyes. The absence of fusion was inferred from the persistence of a large vertical deviation of the eyes (which ranged from 4 to 15°) during binocular viewing (tropia), which was equal to the deviation during monocular viewing (phoria). No vertical fusional movements were observed when the animals fixated a target in the dark or during spontaneous fixation in a lit room. The animals generally fixated with the normal eye but occasionally alternated the fixating eye and foveated the target with the paretic eye for several seconds.
Binocular viewing resulted in a reduction of the amplitude of the monophasic (s-p) drift movements in the paretic eye for monkey IR and reduced the amplitude of the drift components in the paretic eye that followed downward saccades (d-p, s-d) for monkey SO1 (Table 2, Fig. 3; t-test: P < 0.001 for the drift components in both monkeys). In monkey SO1, binocular viewing did not reduce the amplitude of the drift movements in the paretic eye that followed upward saccades (Table 2).
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EFFECT OF BINOCULAR VISION WITH A PRISM.
Eye movements of all three monkeys were studied during a 2-wk period of
binocular viewing with a base-down prism in front of the paretic eye.
The strength of the prism for each animal approximated the size of the
vertical deviation when the normal eye viewed a target straight ahead,
thereby reducing the retinal disparity between the eyes and promoting
binocular fusion. As previously reported, binocular viewing with a
prism led to adaptive changes in the saccadic pulse (an increase in the
size of the pulse in the paretic eye) and adaptive changes in static
alignment (a decrease in the position-dependence of the phoria)
(Lewis et al. 1994).
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EFFECT OF VIEWING WITH THE PARETIC EYE. In one monkey (SO1), eye movements were studied during a 2-wk period of viewing with the paretic eye. In this state, the retina of the paretic eye but not of the normal eye is exposed to the image motion associated with postsaccadic drift. Chronic viewing with the paretic eye caused a reduction of the amplitude of the postsaccadic drift movements in the paretic eye and an induction of upward drift in the normal, covered eye (t-test: P < 0.001 for the changes in both eyes; Table 2, Fig. 7). The upward direction of the drift in the normal eye implies that it resulted from the innervational change that reduced the slow, downward movement (s-d) in the paretic eye.
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Effect of deafferentation of the paretic eye
NORMAL-EYE-VIEWING CONDITION. In all three animals, when the paretic eye was covered with an opaque patch and that eye was deafferented proprioceptively, the vertical postsaccadic drift of the paretic eye was modified by a "directional bias" in the amplitude of the drift movements. This bias in postsaccadic drift generally affected each component of the drift waveform, increasing the amplitude of drift movements in the same direction as the bias and decreasing the amplitude of drift movements in the direction opposite the bias. The direction of the drift bias appeared to be idiosyncratic, however, as it could be directed upward or downward for different animals and saccade directions. For example, in monkey IR, the monophasic postsaccadic drift in the paretic eye was biased upward after deafferentation for both upward and downward saccades [Figs. 8 and 9; t-test: P < 0.001 for (s-p) amplitude]. The amplitude of the drift movements that followed downward saccades also was biased upward in SO1 but was biased downward in SO2 (Figs. 8 and 9; t-test: P < 0.05 for each drift component in both animals). The drift that followed upward saccades was biased down for monkey SO1 (P < 0.001 for each drift component) but was not directionally biased by deafferentation in SO2 (Figs. 8 and 9).
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VISUALLY MEDIATED ADAPTATION AFTER DEAFFERENTATION. Although deafferentation of the paretic eye altered the drift in that eye when it did not receive visual input, deafferentation did not affect the changes in postsaccadic drift that were produced by altering the viewing condition. After deafferentation, chronic binocular viewing without a prism, binocular viewing with a prism, and chronic viewing with the paretic eye resulted in the same pattern of changes in the drift of the paretic eye as occurred predeafferentation (Table 6, Fig. 12). Analysis with a two-way ANOVA indicated that the amplitude of each drift component in the paretic eye was significantly affected by the visual (P < 0.001) and proprioceptive (P < 0.01) states but that no consistent interaction existed between the visual and proprioceptive states.
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DISCUSSION |
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Our results demonstrate several new findings regarding the roles of retinal and proprioceptive afference in the control of postsaccadic drift. When binocular fusion was not possible, retinal slip information from both eyes was an adequate stimulus to promote disconjugate adaptation of postsaccadic drift. When fusion was possible, either retinal disparity or slip could be the dominant visual error signal used to modify postsaccadic eye motion. In addition, proprioceptive deafferentation of the paretic eye altered the amplitude, velocity, and time constant of the postsaccadic drift of that eye but did not influence visually mediated adaptation of postsaccadic drift.
Mechanism of postsaccadic drift
Stability of the eye after vertical saccades requires that the
torques applied to the globe by the four vertically acting extraocular
muscles compensate accurately for the relaxation of the orbital
visco-elastic forces (Goldstein 1983) and for the elastic recoiling forces of the orbital tissues (Robinson
1970
). Postsaccadic drift therefore can occur if the torques
applied to the globe are altered, for example, by changing the strength of an extraocular muscle or by changing the mechanical effect of a
muscle on the globe or if the visco-elastic properties of the
oculomotor plant are modified. In our experimental paradigm, the
superior oblique muscle was paralyzed in two animals, and the
mechanical action of the inferior rectus muscle was reduced in one
animal. Both types of lesions alter the torques applied to the globe
during and after vertical saccades and also change the mechanical
properties of the orbital tissues.
The superior oblique and inferior rectus normally produce different
vertical torques on the globe, and the changes in the visco-elastic
properties of the plant associated with a paresis of the superior
oblique or a tenotomy of the inferior rectus also should be quite
different (Miller and Robinson 1984). Although the
waveform of the postsaccadic drift was the same in the two animals with
superior oblique pareses, the inferior rectus tenotomy and superior
oblique paresis produced different patterns of postsaccadic drift. It
is difficult, however, to correlate specific morphological features of
the composite drift waveforms with the mechanical consequences of the
two lesions (Inchingolo and Bruno 1994
). The rapid drift
movements that immediately follow and are in the direction opposite to
the saccadic pulse (d-p, x-p), in particular, are of uncertain origin.
Similar movements are observed in normal humans and monkeys and are
referred to as dynamic overshoots (Kapoula et al. 1986
).
These movements may be due to a braking pulse supplied by the brainstem
saccadic burst neurons (Van Gisbergen et al. 1981
), or
they may represent a passive response of the ocular motor plant to the
pulse-slide-step of innervation (Goldstein 1987
).
Visually mediated adaptation before deafferentation
DISCONJUGATE ADAPTATION WITHOUT BINOCULAR FUSION.
In the binocular viewing condition, postsaccadic drift in the paretic
eye was suppressed without inducing postsaccadic drift in the normal
eye, despite the absence of binocular fusion. These results indicate
that motion of images on the two retinas is an adequate stimulus to
promote disconjugate adaptation of postsaccadic drift and
that binocular fusion is not mandatory for this process. In contrast,
disconjugate adaptation of the saccadic pulse and static alignment
appears to require binocular foveal (Lewis et al. 1995;
Oohira and Zee 1992
) or perifoveal (Kapoula et
al. 1996a
, 1998
) fusion. These findings are consistent with the
tenotomy studies of Viirre et al. (1988)
, in which
animals with large static deviations (that presumably did not allow
binocular fusion) were able to suppress postsaccadic drift in the
paretic eye with chronic binocular viewing but were not able to
disconjugately adapt their static misalignment or saccadic pulse dysmetria.
DISCONJUGATE ADAPTATION WITH BINOCULAR FUSION. When the animals viewed binocularly with the disparity-reducing prism, two potentially conflicting adaptive stimuli were present after each saccade. The paretic eye was exposed to postsaccadic image motion and a potentially fusible retinal disparity was present. To optimize vision, the animals ideally would minimize retinal slip by reducing the postsaccadic drift of each eye and minimize retinal disparity by moving the eyes toward the alignment where bifoveal fixation is achieved. The two animals with superior oblique pareses (who had large drift movements in the paretic eye but small postsaccadic disparities) responded to the chronic binocular/prism state by suppressing drift in the paretic eye; this led to an increase in the postsaccadic retinal disparity. The animal with the inferior rectus tenotomy (who had large postsaccadic disparities but small drift movements in the paretic eye) responded by moving the eyes toward the alignment that allowed bifoveal fixation, although this required the induction of drift in the paretic and normal eyes for some saccade types.
These results suggest that postsaccadic retinal slip or retinal disparity can be used to adaptively modify motion of the eyes after saccades and imply that the larger of the two visual error signals may dominate the pattern of adaptation. In addition, superior oblique pareses are associated with more prominent cyclodeviation than are pareses of the vertical recti, and the extrafoveal disparity present in the two monkeys with superior oblique pareses could have limited their ability to generate fusional vergence movements. Reduction of postsaccadic retinal slip (which does not require fusion) therefore may have been the primary objective in these animals. In contrast, the monkey with the inferior rectus tenectomy probably lacked a substantial cyclodeviation and hence may have made stronger fusional vergence movements when the vertical deviation was reduced by the prism. In this animal, bifoveal fixation may have been the principle goal, resulting in the induction of postsaccadic drift that reduced the fixation disparity. Previous work in primates suggests that adaptation of the slide and step of innervation minimizes postsaccadic retinal slip but does not correct conjugate or monocular retinal position errors at the end of the saccade (Optican and Miles 1985Effect of deafferentation on postsaccadic drift
Proprioceptive afferents carry information about eye position and
velocity during passive eye motion (Fahy and Donaldson
1998) and could provide the brain with feedback signals that
encode these parameters during volitional eye movements. These afferent signals could function potentially in the immediate, on-line control of
eye movements or could contribute to long-term, adaptive oculomotor control. In the vestibular system of the pigeon, there is evidence that
proprioception functions in an on-line fashion, as passive motion of
the eye modifies vestibular slow phases (Knox and Donaldson 1993
) and deafferentation of the extraocular muscles alters
vestibular eye movements (Hayman and Donaldson 1995
).
In normal monkeys, however, ocular deafferentation does not affect
saccadic eye movements (Guthrie et al. 1983) or the eye position information used to encode visual space in craniotopic coordinates (Lewis et al. 1998
).
In contrast, in monkeys with a vertical muscle paresis, ocular
deafferentation produced a gradual decrease in the amplitude of the
saccadic pulse in the paretic eye (Lewis et al. 1994). In accordance with prior suggestions (Jürgens et al.
1981
; Steinbach and Smith 1981
), we hypothesized
that the feedforward command normally provides the brain with adequate
information for immediate, on-line oculomotor control and that
proprioception provides an error signal used in the long-term, off-line
calibration of the efferent command (Lewis et al. 1994
).
In the current study, we extended our investigation to evaluate the
short and long-term effects of ocular deafferentation on postsaccadic
eye motion in animals with unilateral vertical muscle pareses. The
results indicate that proprioceptive deafferentation modifies
postsaccadic drift in animals with vertical muscle pareses, as the
amplitude, mean velocity, and time constant of the postsaccadic drift
movements in the paretic eye were altered after deafferentation. Postsaccadic drift in the normal eye was not affected by
deafferentation of the paretic eye, despite suggestions that
proprioceptive afference from one eye may affect movements of the other
eye (O'Keefe and Berkley 1991).
EFFECT OF DEAFFERENTATION ON THE STEP AND SLIDE.
As previously described, deafferentation decreased the amplitude of the
pulse in the paretic eye for all vertical saccade conditions except
upwards saccades in monkey SO2 (Lewis et al. 1994). If the step had not been affected by deafferentation,
the change in drift of the paretic eye would have been onward in the direction of the antecedent pulse. This pattern was not consistently observed, suggesting that the drift bias was not simply a passive result of changes in the pulse, but that the step of innervation also
was affected by deafferentation of the paretic eye.
EYE VELOCITY AND POSITION INFORMATION.
Although proprioceptive afferents carry eye velocity and position
signals (Fahy and Donaldson 1998), the changes in
postsaccadic drift that follow deafferentation do not appear to result
from a loss of corrective velocity or position feedback. If
proprioception provided information about postsaccadic eye
velocity that was used to minimize eye motion after
saccades, the velocity and amplitude of the components that make up the
drift waveform should have increased systematically after
deafferentation, but this pattern was not observed.
TEMPORAL COURSE OF CHANGES AFTER DEAFFERENTATION.
Exactly when the bias in postsaccadic drift developed after
deafferentation is uncertain, as it was evident in the first set of
postdeafferentation data recorded 3 days after trigeminal nerve section
and did not change during the subsequent weeks of recording. This
differs from the changes in the saccadic pulse, which evolved during a
period of several weeks after deafferentation (Lewis et al.
1994). These results suggest that proprioception may
contribute to the control of postsaccadic eye motion in a more
immediate, on-line manner or via a short-term adaptive process that is
completed within hours to a few days.
EXPERIMENTAL LESIONS OF THE OCULOMOTOR PLANT. After the trochlear nerve or the inferior rectus tendon was sectioned, the paretic eye drifted after vertical saccades, and the three normal vertically acting extraocular muscles could provide the brain with meaningful proprioceptive feedback about postsaccadic eye motion. Although the quality of the afferent signal from the paretic muscle likely differed in these two experimental models, the consequences of deafferenting the three normal, vertically acting muscles should have been comparable with both lesions.
Because the eye movement data acquired after deafferentation was recorded chronologically later than the predeafferentation data, it is possible that spontaneous, mechanical alterations in the oculomotor plant may have contributed to the changes in postsaccadic drift we observed. Although these mechanical contributions cannot be excluded, the drift components in the paretic eye were not uniformly reduced in amplitude after deafferentation for any monkey or any saccade type. The usual pattern of change was an increase in the amplitude of some drift components and a decrease in others. In some cases, deafferentation was associated with a change in the direction of the postsaccadic drift, which would not be produced by a recovery of eye muscle function.DEAFFERENTATION AND VISUALLY MEDIATED ADAPTATION.
Deafferentation of the paretic eye did not interfere with the adaptive
changes in postsaccadic drift in the paretic eye caused by changing the
chronic viewing state. Furthermore although there is evidence that
proprioception contributes to the binocular coordination of the eyes
(O'Keefe and Berkly 1991), the disconjugate adaptation of postsaccadic drift induced by visual experience also was unaffected by deafferentation. These results are consistent with our finding that
visually mediated adaptation of the saccadic pulse and of the static
ocular alignment does not depend on proprioception from the paretic eye
(Lewis et al. 1994
) and with the finding of
Optican and Miles (1985)
that postsaccadic drift can be
induced adaptively by moving the visual surround after saccades in
normal animals. On the basis of our results, however, we cannot exclude the possibility that deafferentation might have slowed the early rate
of visually mediated adaptation, as we did not record eye movements
until 3 days after the visual state was modified.
Conclusions
In summary, deafferentation of the paretic eye produced a bias in the postsaccadic drift, suggesting that the step was altered, and a change in the time constant of the drift, suggesting that the slide was modified. Visually mediated adaptation of postsaccadic drift was not affected by proprioceptive deafferentation. The direct cause of the changes in postsaccadic drift that occurred after deafferentation is uncertain. Our results are not consistent with the hypothesis that these changes are simply due to a loss of feedback information that is used to minimize postsaccadic eye velocity or to correct errors in eye position. The change in drift after deafferentation appeared to be idiosyncratic, as no consistent pattern occurred that points to an identifiable function for the proprioceptive signal in the control of postsaccadic eye motion (see Table 5).
The finding that visually mediated adaptation was not affected by deafferentation suggests a functional segregation between the afferent retinal and extraretinal signals in the control of eye movements. One possible hypothesis is that proprioception, which transduces length and tension information in the intrinsic coordinates of the eye muscles, provides information that is used by the brain to model the mechanical characteristics of the ocular motor plant. Visual afference, in contrast, provides direct feedback about saccadic accuracy (via the retinal error and retinal slip), and the brain may optimize eye movement control by minimizing these error signals.
Examining larger saccades or saccades in more eccentric orbital positions potentially could help clarify the function of the proprioceptive signal because its role may be more evident when the mechanical nonlinearities of the plant are more prominent. Furthermore examining the early rate of visually induced adaptive changes could be informative because it might be slowed after deafferentation if proprioception provides information that guides the adaptive process (i.e., by signaling the anatomic locus of the abnormality responsible for the eye movement inaccuracy).
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ACKNOWLEDGMENTS |
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We thank D. Roberts, P. Kramer, M. Shelhamer, C. Bridges, and A. Lasker.
This work was supported by National Institutes of Health Grants EY-06273 and NS-01656 to R. F. Lewis and EY-01849 to D. S. Zee.
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FOOTNOTES |
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Present address and address for reprint requests: R. F. Lewis, Massachusetts Eye and Ear Infirmary, 243 Charles St., Boston, MA 02114.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 19 January 1999; accepted in final form 7 May 1999.
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