Department of Surgery (Otolaryngology), University of Mississippi
Medical Center, Jackson, Mississippi 39211
 |
INTRODUCTION |
Visual stabilization mechanisms and labyrinthine
reflexes have evolved to complement each other in maintaining visual
acuity. The primary function of the vestibuloocular reflexes is thus to provide short-latency compensatory eye movements early into the motion,
before visual tracking mechanisms come into play. Accordingly, rotational vestibuloocular reflexes (VOR) originating from the semicircular canals have been shown to operate at very short latencies (~7 ms) (Maas et al. 1989
; Minor et al.
1999
; Tabak and Collewijn 1994
). In primates and
humans, in particular, preattentive visual mechanisms that sense the
pattern of optic flow during translational motion have been shown to
elicit compensatory eye movements at latencies of ~60 ms in monkeys
and ~85 ms in humans (see Miles 1998
for a review). If
visual acuity is to be maintained during translational as it is during
rotational stimuli, translational VORs should also operate at very
short latencies. Other than a recent study during free-fall
(Bush and Miles 1996
), all previous reports have
suggested that translational VORs are characterized by long latencies
(>30 ms) (Bronstein and Gresty 1988
; Bronstein et al. 1991
; Gianna et al. 1997
; Snyder
and King 1992
). If true, this fact would question the utility
of these labyrinthine reflexes in maintaining visual acuity during fast
perturbations. In the present study, we have used abrupt, transient
translational stimuli and fixation at near targets in an attempt to
estimate the response latency of the VORs during both lateral and
fore-aft motions.
 |
METHODS |
Four juvenile rhesus monkeys were chronically implanted
with a head restraint platform and dual coils on each eye. Binocular three-dimensional (3-D) eye movements were recorded inside a magnetic field (CNC Engineering), then calibrated and expressed as rotation vectors (relative to straight-ahead; leftward was positive) (for details see Angelaki 1998
). The motion was delivered by
a whole-body displacement on a sled (Acutronics) either along the
lateral or fore-aft direction. Translational stimuli consisted of a
steplike linear acceleration profile, followed by a short period of
constant velocity (peak linear acceleration: 0.5 G; steady-state
velocity: ±22 cm/s). The stimulus waveform had a frequency content of
<50 Hz. The present analyses are concentrated on horizontal eye
movements elicited during the first 50 ms (~0.25 cm). An identical,
precalibrated search coil that was secured on the head implant measured
negligible head rotation (<0.5°/s) during motion. For lateral
movements, the animals (n = 4) fixated a centered
target (at distances of 40, 30, 20, 15, and 10 cm from the eyes). For
fore-aft motion, the animals (n = 3) fixated one of two
targets at horizontal eccentricities of approximately ±6 cm from the
right eye and a distance of 20 cm
(~17°).1 Each
trial was initiated under computer control only when the animal had
satisfactorily fixated (binocularly) the target. Within a random time
of 2-20 ms after the target light was turned off, positive, negative,
or no motion stimuli were presented in a pseudorandom fashion (similar
results were also obtained when the target remained on and space-fixed
during motion). Responses and the output of a linear accelerometer
mounted on the head were low-pass filtered (200 Hz, 6-pole Bessel) and
digitized (833.33 Hz, 12- or 16-bit resolution). Eye position was
differentiated with a Savitzky-Golay quadratic polynomial with a
1-point forward and backward window (<5% attenuation for frequencies
<50 Hz). Both actual and ideal responses (see next paragraph) were
further processed through digital notch filters (60 and 120 Hz).
For the rotational VOR, latency is usually computed as the difference
between the onsets of eye velocity and head velocity. For the
translational VOR, however, the choice might not seem as
straightforward. A comparison of the onsets of eye position/velocity and linear acceleration is not considered appropriate because of
different waveform and scaling of the two signals (Figs.
1-3). Thus it is necessary to estimate translational VOR latency by comparing
the actual eye movement with an "ideal" (i.e., simulated) response
(computed from the head displacement waveform; see
APPENDIX). The onset of the eye movement was then
calculated for each experimental run in each of the animals, as
follows. First, the preresponse baseline was determined by computing
the mean (±SD) during the 50-ms period immediately preceding sled
motion. Response onset was then computed either by fitting a line to
the data (starting at the point at which the profile first exceeded the
mean baseline by 3 SDs and ending 17 ms later) (Bush and Miles
1996
) or as the time after which the next 5-15 consecutive
data points exceeded the mean baseline by 3 SDs. Because both methods
gave similar results, numbers reported here are based on the latter
method.

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Fig. 1.
Lateral motion: mean (±SD) right eye position (A) and
velocity (B) from at least 40 experimental runs are
compared with ideal responses (dark vs. gray thick lines) during
rightward and leftward motion stimuli (top and
bottom traces, respectively). Positive eye movement is
to the left. Thin vertical dotted lines mark 10-ms intervals. The
single thick vertical dotted line in each plot marks the start of the
stimulus (linear acceleration has been also superimposed in
A). Histograms of latency computed from each individual
run illustrate the mean and median values (thick solid and dashed
lines, respectively). Data from animal 2 at a viewing
distance of 10 cm.
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Fig. 2.
Mean horizontal right and left eye position during rightward and
leftward motion (top and bottom traces,
respectively) at different viewing distances illustrates that viewing
distance dependence was seen with the shortest latency. Dotted lines:
stimulus linear acceleration (peak of 0.5 G). Data from animal
2 (middle target). Notice the conjugate eye movements that are
elicited for viewing distances of 20-40 cm, as compared with rather
disjunctive eye movements for viewing distances of 10 and 15 cm. The
abducting eye (e.g., left eye during rightward motion and right eye
during leftward motion) was always characterized by larger responses
compared with the adducting eye.
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Fig. 3.
Fore-aft motion: mean horizontal eye position (A) and
ideal position (B) during forward (top part of each
plot) and backward (bottom part of each plot) motion for fixation at
~17° to the left (left plots) or to the right
(right plots; animal 2). Thin vertical dotted lines mark
10-ms intervals. The single thick vertical dotted line in each plot
marks the start of the stimulus. The initial portion of stimulus
acceleration is shown as a reference.
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|
As a measure of early reflex gain during lateral motion, we computed
initial acceleration for each run by fitting a line to the first 17 ms
of both actual and ideal eye velocity (shifted by the corresponding
latency). Initial acceleration gain was computed as the ratio of the
slopes of the two lines. Similar values were also obtained by fitting
average response profiles. Because of smaller response amplitudes, only
average response profiles were fitted for fore-aft responses.
 |
RESULTS |
Translational VOR latency
Lateral motion response latencies were estimated by comparing the
onset of eye position and velocity to that of the respective ideal
responses. Computed latencies for each run varied between 8 and 22 ms
with a mean of 11.9 ± 5.4 ms (mean ± SD; Table
1). Similar latency values were also
obtained by examining average response profiles (Fig. 1,
A and B). Even the earliest components of
the response scaled with target distance (Fig. 2). Horizontal eye
velocity for viewing distances of 40 and 10 cm differed by 1 SD as
early as 12.8 ± 3.4 ms (right eye) and 12.6 ± 3.8 ms (left eye).
Forward and backward responses were asymmetric, with latencies being
significantly smaller during forward compared with backward motion
(Table 2;
F(1,766) = 48.2, P
0.01). During
forward motion, latency averaged 7.1 ± 9.3 ms (same for both
eyes). During backward motion, latencies were longer for the abducting
eye (i.e., left eye during left fixation and right eye during right
fixation) compared with the adducting eye (18.9 ± 9.8 ms and
12.5 ± 6.3 ms, respectively; F(1,766) = 27.1, P
0.01). As seen from Fig. 3, the abducting eye
often lagged behind during backward motion and did not start moving
until several milliseconds after the adducting eye.
Initial acceleration gain
Initial eye acceleration gains were generally higher than unity
and consistently larger during forward compared with backward or
lateral motion stimuli (Table 3). The
large initial acceleration gains tended to compensate for the response
latencies such that the early eye movement response approached, albeit
consistently incompletely, that required for maintaining visual acuity
during the movement. In addition, initial acceleration gains were
systematically and consistently higher for abducting than adducting eye
movements. During lateral motion, for example, gains were significantly
higher for the left eye during rightward motion (eliciting a leftward eye movement) and the right eye during leftward motion [rightward eye
movement; F(1,398) = 34.7; P
0.01].
During forward/backward motion where the direction of the elicited eye
movement depends on gaze direction, gains were also higher when the
left eye rotated to the left and the right eye to the right (Table 3).
 |
DISCUSSION |
These results suggest that translational VOR latency might
be as short as that of the rotational VOR. Because of the inherent difficulty associated with converting a head translation to an eye
rotation, we have considered it more appropriate to reference latency
estimates to an "ideal" eye rotation rather than to head acceleration. For lateral motion and fixation at the nearest target, latencies averaged 11.9 ± 5.4 ms. The longer latencies previously reported during lateral motion in humans (~34-60 ms) could be at
least partly due to shallower stimulus profiles and fixation of far
targets (Bronstein and Gresty 1988
; Bronstein et
al. 1991
; Gianna et al. 1997
). The present
values for horizontal eye movement latencies during lateral motion
could be considered similar to those recently reported for vertical eye
movements during free-fall (Bush and Miles 1996
). Long
latencies for the translational VOR were also implied from experiments
using eccentric rotations (Crane et al. 1997
;
Snyder and King 1992
). Because of small linear
acceleration stimuli in these eccentric rotation studies, early changes
in eye velocity could have been difficult to resolve. Moreover, even though it is likely that these rotation axis-dependent components were
at least partly controlled by otolith signals, they might not actually
represent a linear superposition of the translational VORs.
Surprisingly short latencies were also observed during forward
movements (7.1 ± 9.3 ms). Response latencies were usually longer for backward motion. This could reflect a broader adaptation toward forward-directed eye-head coordination tasks that make up the bulk of
visually guided behavior. An unexpected asymmetry was also found in the
movement of the two eyes. Initial acceleration gains were consistently
larger for abducting than adducting eye movements. In contrast,
latencies were longer for the eye in abduction (albeit this difference
in latency was only significant for backward head movements). Although
a functional significance for these differences is unclear, they might
reflect neural constraints in the yet unknown neural elements
generating these responses. The higher initial acceleration gains for
abducting eye movements, for example, could reflect higher gains in
otolith-ocular pathways to the abducens compared with the medial rectus motoneurons.
Despite these asymmetries, the present data suggest that the
short-latency labyrinthine signals could provide for a fast
compensation and improved visual acuity during the early stages of
translatory movements when optic flow visual mechanisms are inoperative.
The "ideal" horizontal eye movement that should be
elicited to maintain visual acuity during translation was computed
based on the head displacement waveform (through a double integration of the linear acceleration stimulus) and on the geometric relationships transforming a head linear displacement into an eye rotation (e.g., Paige and Tomko 1991a
,b
). Briefly, let
RO and
LO be the horizontal Fick angles of the
right and left eyes and dioc be the
interocular distance. Assuming a fixation point on a flat screen at a
perpendicular distance D and a horizontal eccentricity
H (re right eye, positive values to the left), the new
eye position required to maintain fixation during a lateral
(
y) and/or backward (
x)
displacement is easily calculated to be
This work was supported by National Eye Institute Grants
EY-12814 and EY-10851, Air Force Office of Scientific Research Grant F-49620, and a Presidential Young Investigator Award for Scientists and
Engineers (NASA NAG5-3884).
Address for reprint requests: D. Angelaki, Dept. of Anatomy and
Neurobiology, Washington University School of Medicine, 660 South
Euclid Ave., Box 8108, St. Louis, MO 63110.
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.