Download Proprioceptive and Retinal Afference Modify Postsaccadic Ocular Drift

Proprioceptive and Retinal Afference Modify Postsaccadic
Ocular Drift
RICHARD F. LEWIS,1 DAVID S. ZEE,1 HERSCHEL P. GOLDSTEIN,2 AND BARTON L. GUTHRIE3
1
Department 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
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 normaleye–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.
INTRODUCTION
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
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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 manipula-
0022-3077/99 $5.00 Copyright © 1999 The American Physiological Society
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R. L. LEWIS, D. S. ZEE, H. P. GOLDSTEIN, AND B. L. GUTHRIE
tion 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.
METHODS
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.
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).
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
TABLE
1.
Experimental protocol
Visuo-Proprioceptive State
Predeafferentation
Normal-eye viewing (4 wks)
Binocular viewing (2 wks)
Binocular viewing with prism (2 wks)
Paretic-eye viewing (2 wks)
Postdeafferentation
Normal-eye viewing (4 wks)
Binocular viewing (2 wks)
Binocular viewing with prism (2 wks)
Paretic-eye viewing (2 wks)
Monkey
IR, SO1, SO2
IR, SO1
IR, SO1, SO2
SO1
IR, SO1, SO2
IR, SO1
IR, SO1, SO2
SO1
The identified animals were studied in four visual conditions before and
after deafferentation of the paretic eye. The duration of each condition is
indicated in parentheses.
REGULATION OF POSTSACCADIC DRIFT
553
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).
FIG. 1. Representative vertical saccades made by monkeys IR and SO1,
normal-eye–viewing state, predeafferentation, demonstrating the waveforms of
the postsaccadic drift in the paretic eye. Vertical axes indicate vertical eye
position (in °) and corresponding vertical eye velocity (°/s), but the traces have
been offset for clarity. P, pulse; s, step; x and d are inflection points in the drift
movement, as described in the text. Horizontal lines indicate velocity of 0°/s.
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
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 5 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 5 x line.
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 1 be2t/ TC ) to the eye movement trace with the leastsquared-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.
RESULTS
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
FIG. 2. Plots of the average change in postsaccadic drift of the paretic eye
(PE) vs. the average change in the drift of the normal eye (NE) for monkeys IR
(●) and SO1 (n), resulting from the transition from the normal-eye-viewing
(NEV) state to the binocular viewing (BEV) state before deafferentation. Each
icon represents the average change in drift for 1 of the 4 types of saccades
measured and is derived from all of the saccade data recorded in the 2 states
(as displayed in Table 2). Drift measurements of the paretic eye are (s-p) for
monkey IR and (s-d) for monkey SO1. Drift in the normal eye is (s-p) for both
monkeys.
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TABLE
R. L. LEWIS, D. S. ZEE, H. P. GOLDSTEIN, AND B. L. GUTHRIE
2.
Drift amplitudes, predeafferentation
NEV State
Monkey IR
Up 10 to 0 saccades
PE Drift (s-p)
NE Drift (s-p)
0 to up 10 saccades
PE Drift (s-p)
NE Drift (s-p)
Monkey SO1
Up 10 to 0 saccades
PE Drift (d-p)
(s-d)
NE Drift (s-p)
0 to up 10 saccades
PE Drift (x-p)
(d-x)
(s-d)
NE Drift (s-p)
Monkey SO2
Up 10 to 0 saccades
PE Drift (d-p)
(s-d)
NE Drift (s-p)
0 to up 10 saccades
PE Drift (x-p)
(d-x)
(s-d)
NE Drift (s-p)
BEV State
BEV/pr State
PEV State
0.80 6 0.26 (324)
20.03 6 0.18
0.25 6 0.23 (195)
0.07 6 0.21
0.47 6 0.25 (407)
0.59 6 0.21
20.73 6 0.24 (339)
0.03 6 0.20
20.20 6 0.24 (143)
0.13 6 0.29
0.86 6 0.33 (260)
0.48 6 0.33
0.57 6 0.21 (112)
20.64 6 0.24
0.27 6 0.21
0.10 6 0.11 (51)
20.22 6 0.18
0.32 6 0.18
0.00 6 0.10 (57)
20.04 6 0.19
0.27 6 0.15
0.12 6 0.13 (26)
20.28 6 0.18
1.03 6 0.19
20.45 6 0.21 (138)
0.10 6 0.10
20.14 6 0.18
20.06 6 0.17
20.84 6 0.22 (72)
0.01 6 0.04
20.19 6 0.16
0.21 6 0.17
20.53 6 0.23 (91)
0.01 6 0.03
0.00 6 0.14
20.12 6 0.19
20.19 6 0.16 (35)
0.02 6 0.04
20.02 6 0.14
0.37 6 0.18
0.19 6 0.25 (361)
21.63 6 0.34
0.13 6 0.76
0.00 6 0.06 (209)
20.57 6 0.33
0.30 6 0.20
20.08 6 0.11 (471)
0.27 6 0.15
21.54 6 0.27
20.03 6 0.28
20.04 6 0.10 (242)
0.42 6 0.15
20.49 6 0.17
0.13 6 0.25
Average amplitude of the postsaccadic drift movements (in deg) in the paretic eye (PE) and normal eye (NE), normalized by division by the pulse gain for
the antecedent saccade in that eye, in the normal-eye–viewing (NEV), binocular-viewing (BEV), binocular viewing with a disparity-reducing prism (BEV/pr),
and paretic-eye–viewing (PEV) conditions before deafferentation. Values are the means of all saccades recorded in each visual state (during a 4-wk period in
the NEV state and during a 2-wk period in the BEV, BEV/pr, and PEV states). Values are 6SD with the number of saccades in parentheses. Drift components
are defined in Fig. 1.
viewing did not reduce the amplitude of the drift movements in
the paretic eye that followed upward saccades (Table 2).
For both animals, only small changes occurred in the postsaccadic drift of the normal eye in the binocular viewing condition
(Table 2, Fig. 3). Plotting the change in the drift of the paretic eye
FIG. 3. Representative saccades from up 10 to 0° for monkeys IR and SO1
in the normal-eye–viewing (NEV, —) and binocular-viewing (BEV, z z z )
states, before deafferentation of the paretic eye. PE, paretic eye; NE, normal
eye; V, PE 2 NE (vertical vergence trace). Eye traces in this figure (and all
subsequent figures of saccade waveforms) are offset to clearly present the drift
movements and were recorded during monocular viewing with the normal eye.
The position of the normal eye at the end of the saccade approximates the
position of the target. Because the paretic eye is higher than the normal eye in
all animals and visuo-proprioceptive conditions, the vergence (V ) values are
always positive, and the direction of decreasing vergence angle is downward.
Calibration bars for the time and position axes are located in the corner of each
figure.
versus the change in the drift of the normal eye for monkey IR
(Fig. 2) illustrates that chronic binocular viewing resulted in
changes in drift that were disconjugate and primarily affected the
paretic eye. Because the waveform of the postsaccadic drift in the
paretic eye had several components in monkey SO1 (and SO2),
assessing the conjugacy of the drift change induced by binocular
viewing was less straightforward than in monkey IR. As discussed
in the section describing the effect of viewing with the paretic eye,
when the normal eye was habitually patched in monkey SO1, that
eye developed drift directed upward. This suggests that the change
in postsaccadic drift in the normal eye resulted primarily from the
alterations in innervation that suppressed the slow, downward
drift movement in the paretic eye (s-d). Therefore the change in
the (s-d) component of the drift in the paretic eye was used to
quantify the conjugacy of the change in drift in monkeys SO1 and
SO2. Plotting the change in the (s-d) component of drift in the
paretic eye versus the change in drift in the normal eye for monkey
SO1 (Fig. 2) indicates that the changes associated with chronic
binocular viewing were disconjugate but less so than in monkey
IR. The data points are closer to the y axis than the y 5 x line
for SO1 but are further from the y axis than are the data points
for IR.
In summary, despite the apparent absence of fusion,
chronic binocular viewing resulted in a reduction in the
amplitude of postsaccadic drift in the paretic eye for monkey
IR (upward and downward saccades) and SO1 (downward
saccades). The change in postsaccadic drift was disconjugate, as the reduction in the drift of the paretic eye was
REGULATION OF POSTSACCADIC DRIFT
FIG. 4. Representative saccades from 0 to up 10° for monkeys IR and SO2
in NEV state (—) and binocular/prism state (BEV/pr, z z z ) before deafferentation.
accompanied by smaller changes in the drift of the normal eye.
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).
In monkeys SO1 and SO2, chronic binocular viewing with a
disparity-reducing prism resulted in a reduction of the ampli-
FIG. 5. Plots of the average change in the drift of the PE vs. the average
change in the drift of the NE, resulting from the transition from the NEV state
to the BEV/pr state, predeafferentation. Icons represent the 4 saccade types for
monkeys IR (●), SO1 (n), and SO2 (e) and are derived from all of the saccade
data recorded in the 2 states. Paretic eye drift measurements are (s-p) for
monkey IR and (s-d) for monkeys SO1 and SO2.
555
tude of drift movements in the paretic eye that followed downward saccades (d-p, s-d) and reduced the amplitude of the slow,
downward component of the drift (s-d) that followed upward
saccades (Table 2, Fig. 4; t-test: P , 0.001 for these drift
components in both animals). Little change occurred in the
postsaccadic drift of the normal eye (Fig. 5). These changes in
drift reduced the retinal slip of the paretic eye but increased the
amplitude of the postsaccadic fixation disparity in monkeys
SO2 (Fig. 6) and SO1.
In contrast, the changes in drift that occurred in the binocular
viewing/prism state in monkey IR always brought the eyes
toward the alignment that allowed binocular fusion, but in
some cases large drift movements were induced in the paretic
eye. For example, because the effective strength of the prism
increased with upward gaze positions in monkey IR, saccades
from 0 to up 10° required an increase in the paretic eye
hyperdeviation to maintain bifoveal fixation. Chronic viewing
in the binocular/prism condition resulted in the induction of
upward drift in the paretic eye for saccades from 0 to up 10°
(Table 2, Fig. 4), decreasing the postsaccadic retinal disparity.
For monkey IR, the amplitude of the drift in the paretic eye, and
the consequent retinal slip, increased in the binocular viewing/
prism state for three of the four saccades types studied, although the postsaccadic retinal disparity was reduced in each
case (Fig. 6).
In summary, monkeys SO1 and SO2 had large drift movements in the paretic eye but small postsaccadic disparities in
the binocular viewing/prism condition before adaptation, and
FIG. 6. Effect of the adaptation produced by chronic binocular viewing
with a disparity-reducing prism on the postsaccadic drift in the paretic eye,
and on the postsaccadic retinal disparity, predeafferentation. Plotted are the
average values of the PE drift (s-p) and the postsaccade disparity for the 4
saccade types in monkey SO2 (l) and IR (n), PRE (▫ and L) and POST (l
and n) visually mediated adaptation. Postsaccade disparity is determined at
the step position and is defined as (PE retinal error 2 NE retinal error)
while viewing through the base-down prism. Changes in postsaccadic
disparity resulting from visually mediated adaptation are due to modifications in both the saccadic pulse (Lewis et al. 1994) and the postsaccadic
drift.
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R. L. LEWIS, D. S. ZEE, H. P. GOLDSTEIN, AND B. L. GUTHRIE
chronic binocular viewing with the disparity-reducing prism
resulted in a disconjugate reduction of the amplitude of the
postsaccadic drift in the paretic eye but an increase the size of
the postsaccadic fixation disparity (Fig. 6). Conversely, monkey IR had relatively large postsaccadic disparities and small
drift movements in the binocular viewing/prism condition before adaptation and responded to the chronic binocular viewing/prism state by reducing the fixation disparity but generally
increasing the amplitude of the drift in the paretic eye (Fig. 6).
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.
Effect of deafferentation of the paretic eye
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
NORMAL-EYE–VIEWING CONDITION.
FIG. 7. Representative saccades for monkey SO1 in the NEV (—) and
paretic-eye–viewing (PEV, z z z ) states, predeafferentation. Left: saccade from
0 to up 10; right: saccade from up 10 to 0.
FIG. 8. Representative saccades for the 3 monkeys in the NEV predeafferentation (—) and postdeafferentation (z z z ) states. Top: saccades from 0 to up
10°; bottom: saccades from up 10 to 0°.
down for monkey SO1 (P , 0.001 for each drift component)
but was not directionally biased by deafferentation in SO2
(Figs. 8 and 9).
Before deafferentation, horizontal saccades for the three
monkeys were followed by a monophasic postsaccadic drift in
the paretic eye that was in the opposite direction of the antecedent saccade. The amplitude of these horizontal postsaccadic
FIG. 9. Average postsaccadic drift in the PE and NE for each monkey in the
NEV state before (▫) and after (n) deafferentation of the PE. Error bars indicate
1 SD. Displayed data are derived from all of the saccades recorded in the 2
proprioceptive states, and the number of saccades for each state is indicated in
Tables 2 and 6.
REGULATION OF POSTSACCADIC DRIFT
TABLE
3.
557
Drift velocity, normal-eye viewing
Deafferentation
Monkey IR
Up 10 to 0 saccades
0 to up 10 saccades
Monkey SO1
Up 10 to 0 saccades
0 to up 10 saccades
Monkey SO2
Up 10 to 0 saccades
0 to up 10 saccades
Pre
Post
P
5.2 6 1.8 (55)
7.5 6 2.6 (43)
7.5 6 2.8 (71)
4.6 6 1.9 (58)
,0.001
,0.001
2.8 6 0.9 (45)
1.1 6 0.3 (50)
1.9 6 0.8 (45)
2.0 6 0.5 (53)
,0.001
,0.001
3.9 6 1.3 (86)
4.8 6 1.3 (89)
6.1 6 2.1 (82)
5.5 6 1.3 (80)
,0.001
0.005
Mean eye velocity (deg/s) for the paretic eye drift is defined as the average
of the absolute value of eye velocity measured every 4 ms during the 100-ms
period that followed the rapid, initial (d-p, x-p) drift movements. Data are the
average values obtained on day 18 of the normal-eye–viewing state before and
after deafferentation, Values are means 6 SD with the number of observations
in parentheses. P values are from Student’s t-test.
drift movements was generally small (,0.39° for 11 of the 12
saccades studied), but trigeminal nerve section produced small
changes in the amplitude of the horizontal drift in the paretic
eye (,0.2° for 11 of the 12 saccades studied) that were
significant statistically (t-test: P , 0.05).
The effect of deafferentation on the average velocity of
vertical postsaccadic drift in the paretic eye paralleled the
effect on the amplitude of the drift (Table 3, Fig. 9). In monkey
SO2, the net amplitude of the vertical postsaccadic drift increased after deafferentation as did the mean drift velocity. For
monkeys IR and SO1, the net amplitude and mean velocity of
the drift increased for some saccades (for example: IR,10 to
.0; SO1,0 to .10) and decreased for other saccades (IR,0 to
.10; SO1,10 to .0) (Table 3, Fig. 9). The time constant of the
vertical drift movement, when it could be approximated by a
negative exponential [(s-p) for monkey IR; (s-d) for monkeys
SO1 and SO2), became lower after deafferentation of the
paretic eye (Table 4).
The changes in vertical postsaccadic drift that followed
deafferentation were largely limited to the paretic eye for each
monkey; little change occurred in the amplitude of the postsaccadic drift of the normal eye (Fig. 10). Furthermore the
change in the drift of the paretic eye did not develop gradually
after deafferentation; it was evident when the first data after
TABLE
4.
Drift time constants, normal-eye viewing
deafferentation was recorded (3 days after trigeminal nerve
section), and it did not vary substantially over the subsequent
4-wk period of data collection (Fig. 11).
In summary, deafferentation altered the amplitude, velocity,
and time constant of the postsaccadic drift movements of the
paretic eye. The time constants typically were shorter after
deafferentation in all three animals, and the drift bias was
directed upward for all saccade types in monkey IR. No other
consistent pattern to the changes was evident in the three
animals, and no systematic differences occurred between animals with the two types of plant lesions. Deafferentation did
not consistently increase the amplitude of the drift movements
in the paretic eye, did not have a consistent effect on the
conjugacy or position-dependency of the postsaccadic drift,
and did not consistently alter the magnitude or position dependence of the static ocular misalignment (Table 5).
VISUALLY
Deafferentation
Monkey IR
Up 10 to 0 saccades
0 to up 10 saccades
Monkey SO1
Up 10 to 0 saccades
0 to up 10 saccades
Monkey SO2
Up 10 to 0 saccades
0 to up 10 saccades
FIG. 10. Plots of the average change in the postsaccadic drift of the PE vs.
that of the NE resulting from deafferentation of the paretic eye, NEV condition. Drift is defined for these plots as the net change in eye position after the
pulse (s-p). Data are derived from all the saccades recorded in the 2 states. ●,
monkey IR; n, monkey SO1; and l, monkey SO2.
Pre
Post
P
164 6 37 (70)
129 6 35 (38)
170 6 46 (65)
90 6 32 (37)
0.4
,0.001
109 6 22 (50)
123 6 32 (45)
83 6 21 (38)
95 6 20 (38)
,0.001
,0.001
191 6 36 (55)
230 6 34 (53)
134 6 31 (43)
179 6 29 (38)
,0.001
,0.001
Time constant (in ms) for the paretic eye approximated by fitting a negative
exponential to the s-p (IR) and s-d (SO1 and SO2) drift movements. Displayed
are the average values obtained on day 18 of the normal-eye–viewing state
before and after deafferentation. Values are means 6 SD with the number of
observations in parentheses. P values are from Student’s t-test.
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.
The disconjugacy of the changes in drift produced by altering the viewing condition was not affected by deafferentation
in a consistent manner. Before and after deafferentation, the
558
R. L. LEWIS, D. S. ZEE, H. P. GOLDSTEIN, AND B. L. GUTHRIE
DISCUSSION
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
FIG. 11. Postsaccadic drift in the PE for monkey SO1, down 10 to 0
saccades, NEV condition before and after deafferentation (indicated by the
vertical line at day 0). Displayed are the average amplitudes of the drift
components before deafferentation 61 SD (large icons to the left of the vertical
lines), and the average amplitudes recorded in each session after deafferentation (n 5 20 –30 saccades/session), plotted as a function of time after deafferentation. Dotted horizontal lines indicate the average amplitude of each drift
component after deafferentation.
two binocular viewing conditions resulted in changes in the
amplitude of the drift of the paretic eye, but much smaller
changes in the amplitude of the drift of the normal eye (Figs.
2, 5, and 13). The summed square errors about the y (disconjugate) axis in these diagrams were therefore small in both
proprioceptive states (Fig. 14). The conjugacy of the change in
drift produced by chronic viewing with the paretic eye in
monkey SO1, assessed as the summed square error about the
y 5 x (conjugate) axis, was also similar before and after
deafferentation (pre: 0.31 deg2; post: 0.55 deg2).
TABLE
5.
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
Functional effect of deafferentation
Upward Saccades
210 to 0
0 to 10
IR
Drift bias
(s-p) amplitude
Drift conjugacy
Drift pos-dep
u
2
1
2
Phoria size
Phoria pos-dep
1
1
SO1
d
1
2
2
(upward)
2
2
Downward Saccades
0 to 210
10 to 0
SO2
IR
SO1
SO2
IR
*
*
*
*
u
2
1
d
1
2
*
*
*
u
1
2
2
*
*
1
1
2
2
*
*
1
2
SO1
u
1
1
1
(downward)
1
2
SO2
IR
SO1
SO2
d
1
2
1
u
1
2
u
2
1
d
1
2
2
1
1
2
1
2
2
1
Effect of deafferentation of the paretic eye, normal-eye–viewing state. u, up; d, down; 1, increase, 2, decrease; *, no change. Drift pos-dep, positiondependence of the paretic eye drift, defined as the magnitude of the difference in the drift that followed saccades from up 10 to 0 and 0 to down 10 (downward
saccades) and the difference in the drift that followed saccades from down 10 to 0 and 0 to up 10 (upward saccades). Phoria size, amplitude of vertical ocular
misalignment during steady fixation with the normal eye; phoria pos-dep, dependence of phoria size on vertical position of the fixating eye. The calculations for
the table used the average values of all the drift and eye position data collected in the normal-eye–viewing state before and after deafferentation.
REGULATION OF POSTSACCADIC DRIFT
TABLE
6.
559
Drift amplitudes, postdeafferentation
NEV State
Monkey IR
Up 10 to 0 saccades
PE Drift (s-p)
NE Drift (s-p)
0 to up 10 saccades
PE Drift (s-p)
NE Drift (s-p)
Monkey SO1
Up 10 to 0 saccades
PE Drift (d-p)
(s-d)
NE Drift (s-p)
0 to up 10 saccades
PE Drift (x-p)
(d-x)
(s-d)
NE Drift (s-p)
Monkey SO2
Up 10 to 0 saccades
PE Drift (d-p)
(s-d)
NE Drift (s-p)
0 to up 10 saccades
PE Drift (x-p)
(d-x)
(s-d)
NE Drift (s-p)
BEV State
BEV/pr State
PEV State
1.23 6 0.52 (222)
0.25 6 0.25
0.04 6 0.33 (103)
0.45 6 0.21
20.09 6 0.24 (294)
0.48 6 0.22
0.16 6 0.53 (132)
0.07 6 0.34
0.09 6 0.36 (58)
0.19 6 0.30
0.77 6 0.35 (189)
0.19 6 0.25
0.66 6 0.19 (295)
20.42 6 0.21
0.20 6 0.13
0.28 6 0.15 (95)
20.29 6 0.20
0.18 6 0.13
0.02 6 0.09 (117)
20.13 6 0.27
0.27 6 0.13
0.15 6 0.14 (77)
20.28 6 0.14
1.01 6 0.20
20.57 6 0.20 (273)
0.05 6 0.08
20.56 6 0.22
20.14 6 0.15
20.73 6 0.20 (133)
0.01 6 0.04
20.59 6 0.19
20.04 6 0.16
20.49 6 0.20 (180)
0.00 6 0.04
20.23 6 0.18
0.02 6 0.15
20.38 6 0.16 (64)
0.02 6 0.04
20.15 6 0.20
0.09 6 0.18
0.14 6 0.30 (214)
22.18 6 0.49
0.09 6 0.35
0.03 6 0.08 (180)
20.36 6 0.31
0.37 6 0.20
20.06 6 0.09 (279)
0.39 6 0.10
21.73 6 0.27
20.18 6 0.27
20.06 6 0.11 (155)
0.42 6 0.19
20.65 6 0.18
20.23 6 0.25
Average amplitude of the components of the postsaccadic drift movements in the four visual states (as described in Table 2) after deafferentation of the paretic
eye.
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 sup-
plied 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
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 post-
DISCONJUGATE ADAPTATION WITHOUT BINOCULAR FUSION.
FIG.
12. Representative saccades for the 3 monkeys after deafferentation in
the 4 visual states. —, NEV condition; z z z, BEV, BEV/pr, or PEV conditions.
Downward saccades are from up 10 to 0, and upward saccades are from 0 to
up 10.
FIG. 13. Average change in the drift of the PE vs. that of the NE for the 4
saccade types in all 3 monkeys, resulting from the transition from the NEV
state to the BEV state or the BEV/pr state postdeafferentation. Icons are
derived from all the data recorded in these states. ●, monkey IR; n, monkey
SO1; and l, monkey SO2.
560
R. L. LEWIS, D. S. ZEE, H. P. GOLDSTEIN, AND B. L. GUTHRIE
2
FIG. 14. Plots of the summed square errors (in deg ) for the 4 vertical
saccade types, measured about the disconjugate (y axis) and the conjugate (y 5
x line; see Fig. 2), resulting from the transition from the NEV state to the BEV
and BEV/pr states. Filled icons are before and open icons are after deafferentation. Values are derived from the means of all the data recorded in each
visual and proprioceptive state.
saccadic 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.
In normal human subjects, if postsaccadic retinal image
motion is presented to one eye while the other eye views a
stationary, nonfusible pattern, a conjugate pattern of postsaccadic drift adaptation occurs (i.e., changes in drift are approximately equal in the 2 eyes) (Kapoula et al. 1990). These
authors suggested that binocular fusion is required for disconjugate adaptation of drift, although subsequent similar experiments using fusible dichoptic visual stimuli failed to induce
substantial vertical disconjugate postsaccadic drift (Kapoula et
al. 1996b). The reason for the discrepancy between their results
and our findings is uncertain. Although the incongruency between retinal and proprioceptive afferent signals in the paradigm used by Kapoula et al. (1990) may be partially responsible for their findings, we have demonstrated that ocular
deafferentation does not inhibit visually mediated disconjugate
adaptation of drift. Thus this form of oculomotor adaptation
does not require a congruence between retinal and extraretinal
afferent signals.
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
DISCONJUGATE ADAPTATION WITH BINOCULAR FUSION.
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 1985;
Optican and Robinson 1980). Although slow postsaccadic
movements that bring the eye toward the visual target have
been reported in cats, on the basis of their dynamic characteristics, these movements most likely do not result from the
efferent (slide-step) signals that normally control postsaccadic
eye motion (Missal et al. 1993).
During disconjugate adaptation of saccades using optical
devices such as prisms (Oohira and Zee 1992) or anisometropic
spectacles (Lemij and Collewijn 1991), a retinal disparity is
present at the end of saccades, which promotes a postsaccadic
fusional vergence movement. In these studies, disconjugate
postsaccadic movements persisted during monocular viewing
and moved the eyes toward the alignment that was required for
bifoveal fixation during the binocular training. Slow, disconjugate movements therefore can be induced adaptively to correct postsaccadic retinal disparity, but postsaccadic drift movements are not induced adaptively in primates to correct
monocular or conjugate position errors. Because fusional vergence movements occur in response to retinal disparity but are
not produced when the retinal positional errors are conjugate,
these findings suggest that the disconjugate eye movements
observed in monkey IR that reduced the postsaccadic retinal
disparity are due to adaptation involving the vertical vergence
system. These movements may result, for example, if the
animal learned to preprogram a corrective vergence movement
with each vertical saccade (Ygge and Zee 1995).
Effect of deafferentation on postsaccadic drift
Proprioceptive afferents carry information about eye position and velocity during passive eye motion (Fahy and Donald-
REGULATION OF POSTSACCADIC DRIFT
son 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).
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.
The time constant of postsaccadic drift depends on the gain
and time constant of the slide of innervation and on the
mechanical response of the ocular plant to a step of innervation
(Optican and Miles 1985). Assuming that the mechanical properties of the plant were not affected by deafferentation, then the
changes in time constant observed after section of the trigeminal nerve reflect a modification of the gain or time constant of
the slide of innervation.
EFFECT OF DEAFFERENTATION ON THE STEP AND SLIDE.
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 pro-
EYE VELOCITY AND POSITION INFORMATION.
561
vided 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.
We previously demonstrated that the amplitude of the saccadic pulse in the paretic eye decreased after deafferentation
(Lewis et al. 1994), suggesting that proprioception partially
corrected the position-error associated with the gaze shift. If
proprioception provided information about eye position that
was used to modify postsaccadic eye motion to correct errors
in the amplitude of the gaze shift, then deafferentation should
have biased systematically the drift in the direction opposite
the preceding hypometric pulse. This also was not consistently
observed. Our results therefore suggest that whereas proprioception influences the efferent slide and step commands that
follow the saccadic pulse, it does not serve to minimize postsaccadic eye velocity or to correct postsaccadic position error
in a consistent fashion.
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 shortterm 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
562
R. L. LEWIS, D. S. ZEE, H. P. GOLDSTEIN, AND B. L. GUTHRIE
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.
Although proprioceptive and retinal afferent signals interact at the single-unit level in several brain areas involved
in vision and the control of eye movements (Ashton et al.
1984; Donaldson and Long 1980; Lal and Friedlander
1990), our results suggest that proprioceptive and visual
information can act independently in the adaptive control of
eye movements. These findings contrast with results in the
visual system (Buisseret 1995), in which interactions between retinal and extraretinal afference appear to be necessary for the development of properties such as orientation
(Buisseret et al. 1988) and disparity selectivity (Trotter et al.
1993) in cells within the visual cortex.
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).
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.
Present address and address for reprint requests: R. F. Lewis, Massachusetts
Eye and Ear Infirmary, 243 Charles St., Boston, MA 02114.
Received 19 January 1999; accepted in final form 7 May 1999.
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