1Medical Research Council Group in Sensory-Motor Neuroscience, 2Department of Physiology, and 3Department of Ophthalmology, Queen's University, Kingston, Ontario K7L 3N6, Canada
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ABSTRACT |
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Corneil, Brian D., Christine A. Hing, Dorothy V. Bautista, and Douglas P. Munoz. Human Eye-Head Gaze Shifts in a Distractor Task. I. Truncated Gaze Shifts. J. Neurophysiol. 82: 1390-1405, 1999. This study examines two current ideas regarding the control of eye-head gaze shifts. The first idea stems from recent studies involving electrical stimulation in the primate superior colliculus that suggest that a residual feedback of gaze displacement persists for ~100 ms after completion of a gaze shift. In light of this hypothesis, we examined the accuracy of gaze shifts generated very soon after the end of a preceding gaze shift. Human subjects were presented with a visual or auditory target along with an accompanying stimulus of the other modality. The accompanying stimulus appeared either at the same place as the target or at the diametrically opposite position, in which case it was termed a distractor. Subjects often made an incorrect gaze shift (IGS) in the direction of the distractor, followed by a recorrect gaze shift (RGS) in the direction of the target. We found that RGSs were accurately driven to the target, even when they followed IGSs by <5 ms, regardless of the size of the IGS. The second idea is that a gaze shift cannot be cancelled in midflight. The end point of IGSs frequently fell short of the distractor. The dynamics of these movements, and of the head movement components during the IGSs in particular, suggests that these hypometric IGSs were planned for a much larger excursion but were truncated and superceded by the reversing RGSs. These results emphasize that the gaze shifting system can change the desired goal of a gaze shift in midflight and that the superceding movement is accurate regardless of the metrics or timing of the preceding movement.
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INTRODUCTION |
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Gaze shifts are composed of rapid, coordinated
movements of both the eyes (eye-re-head) and head (head-re-space) that
serve to reorient the visual axis in space (eye-re-space). Models of the gaze shifting system generally have been constructed to deal with
one movement at a time (in citing literature in this paper, we refer to
gaze shifts or saccades depending on whether
subjects were or were not able to move their head, respectively). This bias has lead to a common assumption that the gaze shifting system is
"ballistic," in the sense that a movement, once initiated, must be
driven to completion (see Becker 1989 for a thorough
review of this issue). Recently there has been a renewed interest in the performance of the oculomotor system in situations employing multiple stimuli of one or more modalities (Corneil and Munoz 1996
; Driver and Spence 1998
; Findlay
1997
; Frens et al. 1995
; Fuller
1996
; Goldring et al. 1996
; Groh and
Sparks 1996
; Hughes et al. 1994
; Munoz
and Corneil 1995
; Schall and Bichot 1998
;
Walker et al. 1995
, 1997
; Yao and Peck
1997
; Zambarbieri et al. 1997
). In the current
and companion (Corneil and Munoz 1999
) papers, subjects
perform in a multimodal target-distractor experiment (described in the
following text). In this experiment, subjects sometimes generate a
movement sequence in which the first gaze shift is in the direction of
the distractor, followed by a second gaze shift to the target. The two
goals in the current paper are to examine the accuracy of the second
gaze shift in light of recent results from perisaccadic and
postsaccadic stimulation experiments in the primate superior colliculus
(SC) (Kustov and Robinson 1995
; Nichols and
Sparks 1995
; Schlag et al. 1998
); and to examine
the dynamics of the first gaze shift to determine whether this movement was reversed in midflight. We show that the performance of the gaze
shifting system in this task illustrates previously unrecognized capabilities and leads to a more comprehensive understanding of the
neural control of orienting movements.
Early models of saccadic control postulated that saccades were driven
via the comparison of the desired and current eye position within the
head (Robinson 1975). A shortcoming of this model was that oculomotor signals within the brain stem do not encode the position of the target relative to the head but instead encode the
desired change in eye position (see Moschovakis et al.
1996
for review). Subsequent models (Jürgens et
al. 1981
; Scudder 1988
) therefore suggested that
saccades were driven by the comparison of desired and current
displacement in eye position. These latter models necessitated the
existence of a displacement integrator to provide the
feedback of current eye displacement. This displacement integrator must
be reset to zero before any subsequent saccade, otherwise the residual
current displacement feedback could disrupt the accuracy of the next
saccade. Recent experiments using electrical microstimulation in the
primate SC to evoke a saccade either during or shortly after a
naturally generated saccade (Kustov and Robinson 1995
;
Nichols and Sparks 1995
; Schlag et al.
1998
) provided evidence for a gradually resetting displacement
integrator with a reset time constant of ~45 ms. The metrics of the
evoked saccade varied as a function of the amplitude of the natural
saccade and either the intersaccadic interval (Nichols and
Sparks 1995
) or the interval from the onset of the natural
saccade to the onset of stimulation (Kustov and Robinson
1995
; Schlag et al. 1998
).
The majority of naturally generated saccades are separated by enough
time that any purported residual command from the displacement integrator would have long since decayed to zero before the onset of
the subsequent saccade. However, there are a few experimental protocols
employing multiple stimuli capable of eliciting closely spaced
saccades. In the double-step paradigm, a visual target initially is
flashed at one location, and subsequently jumped to a second, final
location (Hallett and Lightstone 1976a,b
;
Wheeless et al. 1966
; see Becker 1989
for
review). Depending on subject instructions and the timing of target
steps, subjects may generate a double-saccade response consisting of a
saccade directed to the initial target location and a second saccade to
the final target location. In a few rare occasions, it has been
reported that the second saccade can follow almost immediately after
the end of the first saccade (Aslin and Shea 1987
;
Becker and Jürgens 1979
; Lévy-Schoen
and Blanc-Garin 1974
; Ottes et al. 1984
).
Goossens and van Opstal (1997)
used the double-step
paradigm to test the predictions of a gradually resetting displacement
integrator and showed that, contrary to the results obtained in SC
stimulation experiments, the second saccade of a double-saccade
response was accurate, even when it followed the initial saccade by
between 30 and 50 ms. However, Goossens and van Opstal
(1997)
did not observe many intersaccadic intervals <30 ms,
when any residual displacement feedback would maximally affect the
metrics of the second saccade. Therefore although their results were
inconsistent with a reset constant of 45 ms, their results still could
be explained by a gradual reset of the displacement integrator, albeit
with a faster time constant.
"Target-distractor" experiments, in which a subject is instructed
to look only to one of two different stimuli, also can be used to
elicit closely spaced saccades or gaze shifts. Reaction times in such
experiments are typically longer than reaction times in double target
experiments requiring only a simple detection process (Findlay
1982; Ottes et al. 1985
). A neglected aspect of
target-distractor experiments is a detailed analysis of movements made
to the distractor instead of the target. Such incorrect gaze shifts (IGSs), as opposed to the correct gaze shifts
(CGSs) that go directly to the target, have been reported in only a few
previous target-distractor experiments (Corneil and Munoz
1996
; Munoz and Corneil 1995
; Ottes et
al. 1985
, 1987
; Viviani and Swensson 1982
), perhaps because other studies examined only movements to closely spaced
visual distractors or to predictable target locations (Walker et
al. 1995
, 1997
; Weber and Fischer 1994
). The
movement pattern of an IGS and the subsequent recorrect gaze
shift (RGS) that drives the gaze to the target are basically
identical to the double-saccade responses in double-step experiments
(Ottes et al. 1985
; Viviani and Swensson
1982
). We have noted that the inter-gaze shift interval between
the end of the IGS and the start of the RGS is quite commonly <20 ms
(Fig. 3 of the current paper, see also Fig. 2B of Munoz and
Corneil 1995
and Fig. 3 of Corneil and Munoz
1996
). One goal of the current paper is to reevaluate the
validity of the gradually resetting displacement integrator using a
target-distractor paradigm that frequently elicits very short
inter-gaze shift intervals.
Another feature we have noted from target-distractor experiments is
that the IGS commonly ends short of the location of the distractor
(Corneil and Munoz 1996; Munoz and Corneil
1995
; Ottes et al. 1985
; Viviani and
Swensson 1982
). The second goal of this paper is to understand
the neural mechanisms underlying such hypometric IGSs. On one hand, it
is possible that the hypometria results from an averaging of the
movements to the distractor and target, as envisioned by Becker
and Jürgens (1979)
for double-step responses or because
the first saccade is part of a preplanned sequence. Alternatively, it
is possible that the hypometria results from a truncation of the IGS
due to a midflight change in the internal representation of target
position (Minken et al. 1993
; van Gisbergen et
al. 1981
). Note that the essential question is whether
hypometric IGSs are completed movements or are interrupted in
midflight. If the latter scenario is true, then the first response is
not ballistic. To distinguish whether hypometric IGSs are completed or
not, we examine their dynamics. If hypometric IGSs are completed movements, then their dynamics should resemble the dynamics of normal,
amplitude-matched gaze shifts. If hypometric IGSs are interrupted in
midflight, then their early dynamics should be typical of larger gaze
shifts driven to the distractor or at least be very different compared
with the dynamics of normal, amplitude-matched gaze shifts.
In the current experiments, subjects are free to move their
heads. The advantages of allowing the subjects to move their heads are
twofold. First, we can examine separately the dynamics of the eye and
head components during IGSs. The eyes and head are very different
mechanical structures, and the dynamics of the head in particular may
reveal more about the initial motor command, given that the head
initially accelerates faster for larger head movements
(Zangemeister et al. 1981). Second, because the head is
unrestrained, we can examine movements of larger amplitude and longer
duration than those studied in previous experiments. Longer duration
gaze shifts presumably have longer intervals over which they can be interrupted.
In our task, a visual or auditory target is presented along with an
auditory or visual accompanying stimulus respectively, either at the
same location (enhancer conditionFig.
1A) or at opposite locations
(distractor condition
Fig. 1B). We have noted before that the number of IGSs generated in the distractor condition depends on the state of visual fixation (Munoz and Corneil
1995
) and on the asynchrony between the presentation of the
target and accompanying stimulus (Corneil and Munoz
1996
). The benefit of using multimodal stimuli is that the
processes responsible for the movement patterns we observe are not
operative only for visuomotor processing but rather are fundamental
processes of the gaze shifting system, regardless of the stimulus
modality to which the movements are directed.
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Some of the results detailed here have been presented earlier in
abstract form (Corneil and Munoz 1994, 1995
;
Corneil et al. 1997a
,b
).
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METHODS |
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Experimental setup
All paradigms were reviewed and approved by the Queen's
University Human Research Ethics Board. Three male subjects (ages 23, 26, and 37) and one female subject (age 23) were informed of the
general nature of the study and consented to participate before the
experiments were initiated. These subjects tended to have a large head
movement contribution during gaze shifts to targets within the
oculomotor range, and as such met criteria for head-movers
(Fuller 1992; Goldring et al. 1996
). We
specifically selected head-movers to examine the dynamics of the gaze,
eyes, and head during gaze shifts. One subject (dm, an
author of this paper) was knowledgeable about the specific goals of the
experiment, and another subject (md) was knowledgeable about
the general goals of the experiment. The remaining subjects,
ks and jb, were naive about the goals of the
study. All subjects generated qualitatively similar patterns of eye,
head, and gaze movements.
Subjects were seated upright in a straight-back chair in the
center of a light-tight, sound-attenuated room and faced a translucent visual screen 86 cm away that spanned ±35° of the central visual field. The screen was illuminated diffusely (~1.0
cd/m2) between trials to prevent dark adaptation.
The experiments were performed in darkness except for the presence of
red light-emitting diodes (LEDs) and silence except for noise bursts
emitted from small speakers. The background lights were extinguished
250 ms before a red LED, referred to as the fixation point (FP0.3
cd/m2; CIE chromaticity coordinates:
x = 0.78, y = 0.21), was back-projected onto the center of the screen signaling the start of a trial. The FP
was illuminated for 1,000 ms and then was extinguished for 200 ms
before the presentation of the peripheral stimuli. During this 200-ms
"gap" period, the subjects were in complete darkness. We used this
gap task to increase the number of IGSs that were generated in the
distractor condition (Munoz and Corneil 1995
). Once
presented, the peripheral stimuli remained on for the remainder of the
trial. The peripheral stimuli consisted of a visual stimulus from a red
LED (4.7 cd/m2; CIE international chromaticity
coordinates: x = 0.73, y = 0.26) and/or
a broadband auditory stimulus from a speaker (74 dB at 4 kHz). The
intensities of the peripheral visual and auditory stimuli were taken
from preliminary experiments, which found that gaze shift reaction
latencies were reduced to a minimum for visual stimuli >0.7
cd/m2 and for auditory stimuli >70 dB
(Corneil and Munoz 1996
). The LEDs and speakers were
mounted into small boxes, which were placed to the left and right at
varying eccentricities along the horizontal meridian (described in the
following text). Subjects were free to adopt any combination of eye and
head movements they desired to perform the gaze shift and were not
given any feedback about the eye-head strategy they employed or about
the accuracy of their gaze shifts.
Experimental paradigms
Subjects were required to perform a series of seven experiments consisting of one control experiment and six multimodal experiments. The purpose of the control experiment was to obtain gaze shifts to visual or auditory stimuli presented alone over a range of eccentricities along the horizontal meridian for comparison with gaze shifts generated in the multimodal experiments. In the control experiment, one of the visual or the auditory stimuli was presented to the left or right. No additional stimuli were presented. The subjects were instructed to look to the presented stimulus as quickly as possible. Within each block of trials, the modality of the target (visual or auditory) and the direction of the target (left or right) were varied randomly trial by trial so that all variations were presented an equal number of times. In different blocks of trials, the stimulus boxes were positioned to the left and right at ~5, 15, 30, 45, and 60° eccentricity relative to the central FP. Subjects completed a block of 60 trials for each stimulus position. We did not obtain control data from subject md at 5° because the scleral search coil broke at the end of the preceding block (see Data collection and analysis).
In the remaining six multimodal experiments, the peripheral stimuli
consisted of both visual and auditory stimuli. Within each experiment,
one stimulus was the designated target, and subjects were instructed to
look to the target as quickly as possible. They were not given any
specific instructions on how to behave with regard to the accompanying
stimulus, although they were informed that it would be presented in
each trial. The modalities of the target and accompanying stimulus were
always different across blocks of trials. Three of the multimodal
experiments employed a visual target with an accompanying auditory
stimulus, and the other three experiments employed an auditory target
with an accompanying visual stimulus. The experiments were run with the
peripheral stimuli at each of ~20, 40, and 60° along the horizontal
meridian for a total of six multimodal experiments (i.e., visual or
auditory target, at each of 20, 40, and 60°). The peripheral stimuli
were presented randomly in one of two conditions. In the
enhancer condition (Fig. 1A), the target and
accompanying stimulus were presented at the same point in space. In the
distractor condition (Fig. 1B), the target and
accompanying stimulus were presented on opposite sides of the vertical
meridian. A set of four asynchronies were introduced between the
presentation of the target and accompanying stimulus in both enhancer
and distractor conditions. The target was presented either 40 ms (Fig.
1A) or 20 ms before the accompanying stimulus, or the
accompanying stimulus was presented either 20 or 40 ms (Fig.
1B) before the target. These asynchronies were used to
reduce the predictability of the presentation of the peripheral stimuli
relative to the disappearance of the central FP. In an earlier study,
we found that the yield of IGSs in the distractor condition was
increased when the accompanying stimulus was presented before the
target (Corneil and Munoz 1996).
All variations within the multimodal experiments (left or right; enhancer or distractor; 4 temporal asynchronies) were interleaved randomly within a block of 160 trials by a 486 computer that controlled the experiment at a rate of 1,000 Hz, and all variations were presented an equal number of times within a single block of trials. Subjects completed two blocks of trials for each experiment. Different experiments were run on different days, although subjects usually completed both multimodal experiments at a given eccentricity on the same day. The selection as to which modality would serve as the target for the first multimodal experiment was varied for different days.
Data collection and analysis
Subjects were positioned in the center of a cube, which
set up rapidly oscillating horizontal and vertical magnetic fields (60 and 90 kHz, respectively; phase-angle system from CNC Engineering). Horizontal gaze (eye position in space) and head (head position in
space) movements were recorded via the magnetic search coil technique
(Robinson 1963) from search coils secured on the eye and
head respectively. For measurement of gaze position, a search coil
embedded in a contact lens annulus (Skalar Instruments) was placed onto
the left or right cornea. To reduce the irritation caused by the search
coil, one to two drops of 0.5% proparacaine hydrochloride was
administered for topical anesthesia before insertion of the coil. The
search coil remained on the eye for a period of ~30 min, and
subsequent drops of the anesthetic were administered as required. This
30-min period was the amount of time it took to calibrate the gaze
signal and run both blocks in one multimodal experiment or all blocks
of the unimodal control experiment. Calibration of the gaze coil was
achieved by having the subject look to visual stimuli on the tangent
screen of known eccentricities while keeping the head still.
Occasionally, the wire loops within the scleral search coil
would break either during the placement or removal of the search coil
or during an experiment (as was the case for subject md
during the control experiments). Depending on how the subject felt and
if the search coil had been on the eye for <30 min, a different search
coil replaced the broken one, and the experiment was continued. After
30 min, the search coil was removed from the subject's eye, rinsed
with hydrogen peroxide and sterile water, and subsequently was placed
on the other eye. A second experiment then was run. For measurements of
horizontal head position, a search coil was taped securely on the
subject's forehead in the frontal plane. The head coil was calibrated
as follows. Before the experimental session, an experimenter wore the
head coil and a helmet on which a laser was mounted securely. The
experimenter then sat in the experimental chair and aligned the laser
spot on targets of known eccentricities. At the completion of the
day's session, both of the subject's eyes were checked for corneal
abrasions. Subject ks developed a corneal abrasion and was
unable to complete the entire series of experiments using the scleral
search coils. For the multimodal experiments at 20°, eye and head
movements for subject ks were recorded with DC
electrooculography and a head potentiometer, respectively, as described
previously (Corneil and Munoz 1996
; Goldring et
al. 1996
).
Horizontal gaze and head positions were digitized at 500 Hz. Digitized
data were stored on hard-disk, and subsequent analysis was performed
off-line on a graphics package designed for the analysis of oculomotor
data on a Sun Sparc 2 workstation. Horizontal eye position (eye
position in the head) was reconstructed off-line by subtracting the
calibrated head signal from the gaze signal. Velocity and acceleration
traces were derived from the eye, head, and gaze position signals by a
low-pass finite impulse response filter (Usui and Amidror
1982), with the
3dB cutoff set at 45.9 Hz. The onset of the
gaze shift was determined when the gaze velocity exceeded 30°/s. The
onset of the eye and head movements during gaze shifts were determined
when the corresponding velocities exceeded 30 and 15°/s,
respectively. Marks were inserted on each trial by a data analyst on
the start, finish, and peak velocity and acceleration of the gaze,
head, and eye movement. The durations of the acceleration period for
the gaze, eye, or head movement were determined as the time from
movement onset to peak velocity, and the duration of the deceleration
period was determined as the time from peak velocity to the end of the
movement. Examples of the marks inserted on a single trial are shown in
Fig. 2. All trials were inspected
visually by a second data analyst to check for errors and to ensure
consistency. Gaze shifts were classified as anticipatory and were
excluded from the analysis if they were initiated <80 ms after the
first presented stimulus (Corneil and Munoz 1996
). This
anticipatory cutoff was derived from a previous set of experiments in
our laboratory in which subjects were instructed to anticipate the
appearance of a visual or auditory stimulus at 20°. Movements that
were initiated <80 ms after target appearance were correct ~50% of
the time, whereas movements initiated >80 ms after target appearance
were correct ~95% of the time. Gaze shifts with reaction times >500
ms after the onset of the second presented stimulus were excluded due
to lack of subject alertness. In total, <1% of gaze shifts were
rejected with these two criteria.
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RESULTS |
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In this paper, we describe the metrics and dynamics of gaze shifts generated by subjects in the distractor condition. We refer to the accompanying stimulus presented opposite the target as the "distractor," although the distractor and enhancer conditions were interleaved randomly within each experiment so the accompanying stimulus is technically not a distractor in the enhancer condition. For brevity, we refer to experiments using a visual target and an auditory distractor as VisT/audD experiments, and the converse as AudT/visD experiments. If the location of the stimuli is relevant, the terminology AudT60°R/visD60°L is used to denote trials wherein an auditory target was presented 60° right and a visual distractor was presented 60° left.
Classes of gaze shifts in the distractor condition
Gaze shifts generated by subjects in the distractor condition were
divided into one of two classes depending on the direction of the
initial gaze shift with respect to the location of the target. Figure
3A shows traces of gaze shifts
generated by subject md in VisT60°L/audD60°R trials. The
subject performed the task correctly and generated CGSs by shifting
gaze directly to the target (Fig. 3A, ). He also generated
IGSs by shifting gaze initially in the direction of the distractor
(Fig. 3A, - - -). IGSs were followed very shortly by RGSs,
which brought the subject's gaze to the target. The shorter reaction
times of IGSs compared with CGSs, and the increased number of IGSs
generated when the distractor was presented before the target have been
described in detail (Corneil and Munoz 1996
). These
relationships were observed in the present study for all multimodal
experiments at all stimulus eccentricities and were not studied in
further detail.
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The percentages of IGSs generated by each subject in the distractor conditions of the different multimodal experiments are shown in Table 1. The results are pooled across direction for all subjects (no difference in number of IGSs generated to the right or left, paired t-test, P = 0.60). On average, subjects generated IGSs in 20-30% of all distractor trials (minimum 9%, maximum 63%) in both types of multimodal experiments. In total, we recorded 499 IGSs in VisT/audD experiments and 390 IGSs in AudT/visD experiments.
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Timing and metrics of IGSs and RGSs
Examples of IGSs and subsequent RGSs generated by subject md are shown aligned on target onset in Fig. 3B. A cursory examination of this figure reveals considerable variations in the reaction times and amplitude of the IGSs. Furthermore the subsequent RGS brought gaze to approximately the same location.
To begin to examine the validity of the purported gradually resetting
displacement integrator during IGS-RGS sequences, we first establish
whether the correlations between various metrics during the IGS-RGS
sequences resemble those previously reported in double-step experiments
(see Fig. 3C for a graphic depiction of the parameters). We
measured the reaction time of the IGS relative to target onset because
this time is analogous to the "modification time" concept developed
in double-step experiments (Becker and Jürgens
1979; Lisberger et al. 1975
). The results are
pooled across direction for all further analyses (a series of paired t-test for all subjects in all multimodal experiments
compared either the IGS reaction time, IGS amplitude or inter-gaze
shift intervals for rightward and leftward directed IGSs; in all cases, P > 0.40).
The IGS reaction times, IGS amplitudes, and inter-gaze shift intervals for subject md for multimodal experiments at 40° are shown in Fig. 4, A-C, respectively, and a full breakdown of the parameters of the IGSs is shown for all subjects in all multimodal experiments in Table 2. There were some systematic variations in these parameters depending on either the modality of the target and distractor (i.e., in either VisT/audD or AudT/visD experiments) and on the eccentricity of the stimuli (i.e., at 20, 40, or 60°). A full analysis of these variations departs from the goals of this paper, hence we only briefly summarize the major trends in the data. IGS reaction times tended to be longer in AudT/visD experiments and for distractors placed at 60° [2-factor ANOVA across distractor modality (visual or auditory, P < 0.0005) and distractor eccentricity (P < 0.0005); and by Newman-Keuls post hoc analyses; a significant interaction effect also was revealed (P < 0.0005)].
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IGSs varied widely in amplitude (Fig. 4B). They tended to be smaller in VisT/AudD experiments and when distractors were less eccentric [2-factor ANOVA across distractor modality (P < 0.0005) and eccentricity (P < 0.0005), and by Newman-Keuls post hoc analyses; a significant interaction effect across factors was also revealed (P < 0.0005)]. We distinguished between hypometric IGSs and completed IGSs, depending on how close the IGS brought gaze to the location of the distractor. The cutoff between hypometric and completed IGSs was computed by subtracting two SD from the average of the distribution of CGS end points in the converse experiment when the distractor served as the target. IGSs that fell short of this cutoff were termed hypometric IGSs; the rest were termed completed IGSs. This cutoff for subject md is marked in Fig. 4B (- - -). Percentages of hypometric IGSs are listed for all subjects in Table 2. Significantly more hypometric IGSs were generated in VisT/audD experiments than in AudT/visD experiments (paired t-test, P < 0.05). The distinction between hypometric and completed IGSs is relevant in the section examining IGS dynamics.
The inter-gaze shift interval between the end of the IGS and start of the RGS was highly variable, ranging from <5 to >300 ms (Fig. 4C, Table 2). This inter-gaze shift interval tended to be shorter in VisT/audD experiments and with more eccentric distractors [2-factor ANOVA across distractor modality (P < 0.0001) and eccentricity (P < 0.0001), with Newman-Keuls post hoc analysis; a significant interaction effect between factors was observed (P < 0.0001)].
IGS amplitude (Fig. 5A) and
inter-gaze shift interval (Fig. 5C) tended to be smaller and
shorter for longer IGS reaction times (also see Fig. 3B).
These trends were consistent for all subjects in all multimodal
experiments (24 combinations in all: 4 subjects; 20, 40, or 60°;
VisT/audD or AudT/visD experiments; Fig. 5, B and
D). The observed correlations were stronger and more likely to reach significance in VisT/audD experiments, possibly due to the
greater number of IGSs. These results are analogous to the amplitude-transfer functions described by Becker and
Jürgens (1979), suggesting that a similar mechanism
underlies double-saccade responses in double-step experiments and
IGS-RGS sequences.
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The amplitude of RGSs scaled well for the amplitude of the preceding
IGSs for all subjects (Fig. 6,
A and B), even for inter-gaze shift intervals
approaching zero. The error at the end of the RGS was obtained by
subtracting the RGS end point from the mean end point of all CGSs
generated in the distractor condition in the same experiment (CGSs from
the enhancer condition were not used as they may have been influenced
by the accompanying stimulus). The remaining error at the end of the
RGSs did not differ significantly from the error distribution at the
end of CGSs (data pooled across all subjects and multimodal
experiments, t-test, P = 0.41). More importantly, the error at the end of an RGS did not vary as a function
of the inter-gaze shift interval (Fig. 6C). Systematic overshoots of the RGSs would have been predicted if the purported displacement integrator gradually resets during the inter-gaze shift
interval. The logic for this is as follows. Consider the case in which
target and distractor are placed at 40° to the right and left
respectively. Following a 10° IGS to the left, the gaze shifting
system needs to move 50° to the right to get on target. Assuming that
the gaze shifting system encodes this 50° rightward RGS, as opposed
to the original 40° gaze shift to the target or to some intermediary
location which compensates for any residual decay, then the predicted
amount of error at the end of an RGS due to residual feedback within
the displacement integrator is given by the equation
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(1) |
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The plausibility of the above assumption is considered further in
the discussion. We initially set the value of the decay constant at 40 ms, which is at the low end of values determined from SC stimulation
experiments (Kustov and Robinson 1995; Nichols and Sparks 1995
; Schlag et al. 1998
) and results
in a faster decay of the resettable integrator. Using Eq. 1,
we determined the predicted error for each RGS based on the amplitude
of the preceding IGS and the inter-gaze shift interval and compared
this predicted RGS error to the observed RGS error as a function of the
inter-gaze shift interval (Fig. 6D). We limited our error
predictions to those RGSs that followed an IGS >5° and were preceded
by an inter-gaze shift interval of <150 ms, as the predicted errors in
cases beyond these limits would be negligible. As shown in Fig.
6D, there is a large difference between the observed and
predicted RGS errors, particularly for inter-gaze shift intervals <50
ms. The appreciable scatter in the predicted RGS error for similar
inter-gaze shift intervals occurs because of the variability in the
amplitude of the preceding IGS. We computed the residue as the
difference between the actual and predicted RGS errors and plotted this
residue as a function of inter-gaze shift interval for all subjects in
VisT/audD experiments at 40° in Fig. 6E for
= 40 ms. As shown by the large residues <0, the observed RGS error clearly
departed from the predicted RGS error (Fig. 6E). We repeated
these calculations with
= 10 ms to test whether the observed
RGS accuracy could be explained by a faster decay constant (Fig.
6F). There remained a very large discrepancy between the
predicted and observed RGS errors, particularly for inter-gaze
shift intervals <30 ms. These behavioral results confirm the
conclusions of Goossens and van Opstal (1997)
by
demonstrating the insufficiency of a gradual decay with
= 40 ms in accounting for RGS accuracy and extend on their results by
demonstrating that a decay with
= 10 ms is also insufficient
to account for the accuracy of RGSs.
Dynamics of IGSs
The second goal of this paper was to resolve whether hypometric IGSs that ended short of the location of the distractor were driven to completion. A key part of the following analyses centers on the comparison of "amplitude-matched" movements. Consider the case when the stimuli were located at 40° and the subject first generated a 10° IGS toward the distractor, followed by a 50° RGS in the opposite direction. If the 10° IGS is driven to completion, then its dynamics should be comparable with the dynamics of other, normal 10° gaze shifts. However, if the 10° IGS is initially planned for an excursion of 40° and superseded by the RGS in midflight, then the early dynamics of the 10° IGS should either be similar to 40° gaze shifts, or atypical of normal 10° gaze shifts. Furthermore if the RGS actively supersedes the ongoing IGS, it is possible that amplitude-matched hypometric IGSs and completed IGSs would differ in their decelerations because the hypometric IGSs would be actively reversed by the RGSs, whereas completed IGSs would be stopped in a normal fashion.
The main sequence relationship relates the amplitude and peak velocity
of a gaze shift (Bahill et al. 1975). If the peak
velocities during hypometric IGSs are greater than the peak velocities
attained during amplitude-matched completed IGSs or control gaze
shifts, then the main sequence relationships for hypometric IGSs should lie above the relationships for the other types of movements. Figure
7, A and B, shows
scatter plots of peak gaze velocity as a function of gaze amplitude for
subject dm during hypometric IGSs, completed IGSs, or
control gaze shifts to either auditory (Fig. 7A) or visual
(Fig. 7B) stimuli. The gaze main sequence relationships for
this subject and for the other three subjects were not consistently
different for the three types of gaze shifts.
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Main sequence relationships do not provide a complete description of
the gaze shift dynamics because they do not provide any quantitative
description of either the acceleration or deceleration phases
(van Opstal and van Gisbergen 1987). To more thoroughly examine the dynamics of these movements, we constructed phase-plane plots that relate the position and velocity at every point in time
during a gaze shift. Phase-plane plots for subject dm are shown in Fig. 7, C-E, for leftward gaze shifts directed to
auditory stimuli. Figure 7C plots the phase-plane
relationships for all leftward hypometric (long dashed lines) and
completed (short dashed lines) IGSs generated in VisT40°L/audD40°R
trials. The phase-plane trajectories of gaze shifts >25° could be
divided roughly into three parts: an initial acceleration portion
speeding gaze near to its peak velocity, a middle plateau portion in
which the velocity of the gaze shifts is relatively constant between
300 and 500°/s, and a final deceleration portion near the end of the
movement. The phase-plane profiles of the IGSs (Fig. 7C) can
be contrasted with those for control gaze shifts (Fig. 7D)
generated by the same subject to auditory targets located at different
leftward eccentricities. Notice that the initial accelerations of these control gaze shifts resemble the accelerations of both hypometric and
completed IGSs. However, control IGSs tended to have a more gradual
deceleration than hypometric IGSs [compare the decelerations of
movements ~20° for hypometric IGSs (Fig. 7C) and control
gaze shifts (Fig. 7D)].
Amplitude-matched movements of ~40° are contrasted directly in Fig. 7E for control gaze shifts (solid lines), hypometric IGSs (long dashed lines), and completed IGSs (short dashed lines). The control gaze shifts and the completed IGSs were both driven to auditory stimuli located at 40°, whereas the hypometric IGSs were generated when an auditory distractor was located at 60°. Qualitatively, these three types of movements have similar acceleration trajectories. Although the hypometric IGSs reached higher peak velocities in the examples shown, the more important feature is that hypometric IGSs tended to decelerate more abruptly than either control gaze shifts or completed IGSs.
To quantify these observations, we measured a number of movement
parameters to describe the dynamics of either the acceleration phase
lasting from gaze shift initiation to peak velocity or the deceleration
phase lasting from peak velocity until the gaze shift end. For each
gaze shift, we measured the peak acceleration and deceleration, the
duration of the acceleration and deceleration phases, and the ratio of
the acceleration duration to the deceleration duration. The
acceleration/deceleration duration ratio is one method of extracting
information about the "skew," or shape, of the velocity-time
profile of the movements (van Opstal and van Gisbergen
1987) and allows us to collapse results across subjects. The
peak acceleration (Fig. 8A)
and the duration of the acceleration phase (Fig. 8C) for
each of the three types of gaze shifts were similar for
amplitude-matched movements. However, the peak deceleration tended to
be much higher for hypometric IGSs as compared with either
amplitude-matched control gaze shifts and completed IGSs (Fig.
8B), and the duration of the deceleration phase was
correspondingly shorter (Fig. 8D). The deceleration dynamics
of completed IGSs also tended to be more rapid compared with control
gaze shifts. The values of the acceleration/deceleration duration ratio
derived from hypometric IGSs were significantly higher than the ratios from either completed IGSs or control gaze shifts for subject dm (Fig. 8E) and for all subjects [Fig. 8F;
2-factor ANOVA across distractor modality (P < 0.0001)
and movement type (hypometric IGSs, completed IGSs or control gaze
shifts; P < 0.0001); Newman-Keuls post hoc analysis].
The large differences in the deceleration dynamics of hypometric IGSs
compared with amplitude-matched completed IGSs suggests that hypometric
IGSs are stopped by a different mechanism compared with either
completed IGSs or control gaze shifts. These observations are
consistent with the notion that hypometric IGSs initially were planned
for a larger excursion but were truncated in midflight by the reversing
RGSs.
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Dynamics of eye and head movements during IGSs
We also studied the dynamics of the underlying component movements
of the eyes and head during IGSs. The head, being a viscoinertial structure, must accelerate more rapidly for larger head movements (Zangemeister et al. 1981). Thus the initial dynamics of
the head movement component should be particularly illustrative of the amplitude of the initially desired head movement. Indeed, the dynamics
of the head movement during hypometric IGSs strongly suggested that the
head movement began on a trajectory typical of a much larger movement
but was abruptly reversed by the head movement during the RGS. The main
sequence relationships for the head movement component during aurally
guided gaze shifts for subject dm (Fig.
9A) show that for head
movements of similar amplitudes, the peak head velocity was greater
during hypometric IGSs than during either completed IGSs or control
gaze shifts. This pattern was observed frequently in other subjects for
both visually and aurally guided gaze shifts, although it was not
observed for subject dm during visually guided gaze shifts
(Fig. 9B). Phase-plane relationships for head movement
components during control gaze shifts and completed IGSs tend to be
quite parabolic (Fig. 9, C and D). Peak head
velocity and acceleration increased for larger head movements (Fig.
9D) and did not saturate at larger movement amplitudes. The
phase-plane traces for head movements during hypometric IGSs depart
quite markedly from this parabolic shape and adopt a much more skewed appearance (Fig. 9E, arrows). This skewed appearance
resulted mainly from an abrupt deceleration phase (Fig.
10, B and D),
although the head also accelerated faster during hypometric IGSs (Figs. 9E and 10, A and C). The shorter
deceleration phases resulted in duration ratios that were significantly
greater for head movements during hypometric IGSs compared with head
movements during either completed IGSs or control gaze shifts [Fig.
10E for subject dm, Fig. 10F for all
subjects; 2-factor ANOVA across distractor modality (P < 0.0001) and movement type (P < 0.0001);
Newman-Keuls post hoc analysis].
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|
In contrast to the head movement component, the eye movement component did not systematically differ during the different types of gaze shifts. Main sequence relationships for the eye movement (Fig. 11, A and B) showed that the only notable differences between types of gaze shifts were that some subjects tended to generate much larger eye movements during control gaze shifts than they did during the multimodal experiments (i.e., see Fig. 11A), implying a greater contribution of the head during gaze shifts in multimodal experiments. The phase-plane plots for the eye movement component during IGSs are compared with those from control gaze shifts in Fig. 11, C-E, for subject jb. These phase-plane plots tended to be much more parabolic than the phase-plane plots for gaze shifts and displayed prolonged deceleration phases only for movements >20° (Fig. 11, C and D). There were no systematic differences in the phase-plane plots for the eye movement component during control gaze shifts, hypometric IGSs and completed IGSs for eye movements around 15° (Fig. 11E). Quantitatively, the acceleration and deceleration phases of the eye movement component during gaze shifts were fairly similar during hypometric IGSs, completed IGSs, and control gaze shifts (Fig. 12, A-D), although there was a tendency for the peak eye deceleration to be higher and the duration of the eye deceleration to be lower during hypometric IGSs than during complete IGSs or control gaze shifts when the eye movement exceeded 30° (Fig. 12, B and D). The acceleration/deceleration duration ratios (Fig. 12E for subject jb, Fig. 12F for all subjects) did not reliably discriminate the eye movement during hypometric IGSs from the eye movement during completed IGSs or control gaze shift [2-factor ANOVA across distractor modality (P < 0.0001) and movement type (P < 0.0001)]. Post hoc analysis (Newman-Keuls) revealed that the ratios were not significantly different during hypometric IGSs and control gaze shifts.
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DISCUSSION |
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The results presented in this paper demonstrate that reversing
gaze shifts generated in a multimodal target-distractor experiment are
accurate regardless of the amplitude of the initial, erroneous gaze
shift and of the inter-gaze shift interval. These results complement
and extend on the behavioral results of Goossens and van Opstal
(1997) in double-step experiments by demonstrating accuracy
even when the subsequent gaze shift essentially supercedes and reverses
an on-going gaze shift in midflight. These results impose new
constraints on models of gaze control, which now must be capable of
generating such movement sequences.
We employed some experimental manipulations to increase the
number of IGSs available for study. First, we introduced a 200-ms gap
between the disappearance of the central fixation point and the
presentation of the peripheral stimuli. This manipulation has been
shown to reduce reaction times and increase the incidence of IGSs
compared with when the fixation point remained illuminated (Munoz and Corneil 1995). Second, we introduced
asynchronies between the presentation of the target and distractor to
decrease the predictability of stimuli appearance relative to fixation
point offset. We have shown that the incidence of IGSs displays a
straightforward dependency on the introduced asynchrony; more IGSs are
generated the sooner the distractor is presented relative to the target (Corneil and Munoz 1996
). Third, we allowed subjects to
move their heads, which enabled us to study movements out to 60°
eccentricity. Larger amplitude gaze shifts last longer (Guitton
and Volle 1987
), which increases the possibility of gaze shifts
being truncated in midflight.
Feedback of gaze position and/or displacement
The accuracy of the RGSs in our behavioral task would not have
been predicted if the purported resettable displacement integrator was
endowed with a gradual reset with a time constant in the order of 40 ms. Rather, the models developed from postsaccadic stimulation within
the superior colliculus (SC) (Kustov and Robinson 1995; Nichols and Sparks 1995
; Schlag et al.
1998
) would have predicted the RGS to grossly overshoot the
target (Fig. 6, C-E). The notable accuracy of the many RGSs
that followed inter-gaze shift intervals of <30 ms also runs counter
to the predictions of a faster decaying resettable integrator (i.e.,
= 10 ms), which could not be addressed by the results obtained
by Goossens and Van Opstal (1997)
(Fig. 6F).
Our results are not also consistent with an alternative proposal of an
instantaneous reset of the displacement integrator linked to the end of
a saccade (Moschovakis 1994
), given that hypometric IGSs
are essentially truncated in midflight and hence never reached completion.
How then can the discrepancy between the results from behavioral
experiments and stimulation experiments be accounted for? One unlikely
possibility noted by Goossens and van Opstal (1997) was
that the natural, accurate second saccade they observed was preprogrammed and accommodated for the properties of a gradually resetting displacement integrator. If this was true, the noted changes
in the evoked vector from postsaccadic SC stimulation experiments
occurred because the second saccade, imposed by the experimenters, was
not able to accommodate for the residual displacement feedback. We
consider this scheme unlikely to explain the IGS-RGS sequences because
such preprogramming would be computationally very difficult given that
neither the amplitude of the IGS nor the inter-gaze shift interval,
which together determine the amount of compensation required, would be
known beforehand for any accommodating mechanisms. Furthermore recent
data recorded from the SC in monkeys performing the double-step task
shows no evidence for any dynamic remapping of the SC motor command
that would have to underlie such compensation (Goossens
1998
). The SC appears to encode faithfully the vector of the
impending saccade by always recruiting the same cells at the same SC
locus for the same movement, regardless of the time elapsed since the
end of the preceding saccade. Thus it is reasonable for us to assume
that the population of SC cells active for an RGS is the same
population of SC cells normally active for gaze shifts with the same metrics.
Alternatively, the discrepancy between the accuracy of closely spaced
movements generated naturally or electrically could occur simply
because electrical stimulation does not activate the SC or other
components of the gaze shifting system in a natural manner. Given the
behavioral results presented here and in Goossens and Van Opstal
(1997), the validity and existence of a gradually resetting
displacement integrator in the gaze shifting system must be questioned.
Clearly, some feedback of current eye position or displacement must be available at the time of the RGS generation to account for the amplitude of the preceding IGS. Our data cannot distinguish whether such feedback is operating within a positional or displacement framework. However, if the neural correlate of the displacement integrator does exist, our data shows that it must somehow be instantaneously reset to zero, perhaps by the truncating RGS command, instead of an end of saccade command.
Metrics and dynamics of hypometric IGSs
Many similarities exist between the parameters of the initial
response in the double-saccade or IGS-RGS movement patterns. Results
from double-step experiments first described "amplitude-transfer" functions, in which the amplitude (Becker and Jürgens
1979) or direction (Aslin and Shea 1987
) of the
first saccade of a double-saccade response varied as a function of the
modification interval (the time from the 2nd target step until the
initiation of the 1st saccade). The inter-saccadic interval also was
found to vary as a function of the modification interval, tending to
decrease for longer modification intervals. Similar quantitative
observations have been made in the current report (Fig. 5) and for
errors generated in cueing experiments, in which a cue presented before
a target draws attention, sometimes incorrectly, to the impending
target location (Cavegn 1996
). Errors very similar to
IGSs also are frequently reported in antisaccade trials in which
subjects are instructed to generate a saccade to a spatial location
diametrically opposite the location of a peripheral visual stimulus
(for review, see Everling and Fischer 1998
). Such
erroneous prosaccades can be of intermediate amplitude, and the time
between the erroneous pro-saccade and the subsequent antisaccade can
approach zero (Amador et al. 1998
). However, such
movement sequences are rare (<1%) and therefore have not been studied
in a quantitative manner. Still, the notable similarities between the
movement patterns generated in different experimental protocols are
suggestive of a common neural mechanism.
We have demonstrated that hypometric IGSs are not completed movements
generated from averaging or sequencing mechanisms (see INTRODUCTION), but rather are interrupted in midflight. The
critical determinant of the hypometria of IGSs [and indeed whether
IGSs are generated at all (Corneil and Munoz 1996)] is
the timing of the motor program encoding the RGS with respect to the
motor program encoding the IGS. If the motor program encoding the RGS
is signaled almost immediately after the initiation of an IGS, then the
IGS will most likely be interrupted in midflight by the RGS and the inter-gaze shift interval will correspondingly be short. Alternatively, if the motor program encoding the RGS is delayed until well after the
onset of the IGS, then the IGS will most likely be driven to completion
and the RGS will only be generated after a longer inter-gaze shift
interval. A potential explanation for the paucity of shortened
erroneous prosaccades in antisaccade trials is that the motor program
for the antisaccade lags too far behind the stimulus-driven erroneous
prosaccade to exert any influence, given the added complexity of
determining the metrics of the antisaccade based on the location of the target.
To our knowledge, our study is the first attempt to quantify the
dynamics of the gaze, eye, and head during the first, erroneous response. The dynamics of deceleration of the gaze and head during hypometric IGSs clearly depart from appropriate trajectories for amplitude-matched movements (Figs. 7, C-E, 8, 9, C-E, and 10) and were consistent with the premise of the
head being programmed for a much larger excursion than it achieved
(Figs. 9 and 10). This latter point emphasizes why it was important for
the subjects in the current experiment to be allowed to move their
heads. The acceleration profile of the head is much more illustrative
of the initial motor command than movements of either the eye or gaze,
given that the early part of any gaze shift is driven predominantly by
an eye movement. The dynamics of the acceleration phase remain fairly
constant for eye or gaze movements >10° (Bahill et al. 1981; Fricker and Sanders 1975
), whereas the
head accelerates more rapidly for progressively larger movements (Fig.
10A for head movements during control gaze shifts) (see also
Zangemeister et al. 1981
). Assuming that the eyes and
head are driven by a common signal at some point (note that if this
common signal is within a feedback loop or not is irrelevant), it is
clear that the IGS motor command encoded a gaze shift to the
distractor. It will be of interest to determine whether a similar
analysis of the dynamics of the initial response in double-step,
cueing, or antisaccade experiments is consistent with the preceding explanation.
One obvious limitation of our study is that the support provided for a
neural mechanism in which one motor program can truncate another in
midflight may apply only for stimuli placed in opposite hemifields. It
remains possible that an averaging scenario envisioned by Becker
and Jürgens (1979), or a type of sequential planning, may
apply for stimuli within the same hemifield or placed closer together.
We note the conclusions reached by Minken and colleagues (1993)
who studied the three-dimensional trajectories of eye
saccades in a double-step experiment to targets within the same
hemifield. They showed that the torsional trajectory of curved saccades
modified in midflight were not consistent with an averaging process but rather were consistent with a midflight change in the goal of the gaze
shifting system. However, some of the results observed by these authors
were also indicative of an averaging response, so the phenomena of
averaging and midflight changes may not be mutually exclusive.
We conclude that the oculomotor system is capable of changing its goal
in midflight and that the accuracy of subsequent gaze shifts is
achieved regardless of the amplitude of preceding truncated gaze shift
or of the inter-gaze shift interval. The discrepancy between our
behavioral results and those predicted from electrical stimulation
experiments emphasizes the need for caution in interpreting results
from electrical stimulation. IGSs are overt manifestations of a
distraction process. In the companion paper (Corneil and Munoz
1999), we show that the distractor also can induce early movements of the head before the initiation of a gaze shift.
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ACKNOWLEDGMENTS |
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We thank Drs. I. Armstrong, S. Everling, M. Paré, and S. Scott as well as A. Bell, M. Davidson, and M. Dorris for comments on an earlier draft of this paper. We also acknowledge the helpful comments of the two anonymous reviewers.
This work was supported by a Group Grant from the Medical Research Council of Canada (MRC). B. D. Corneil was supported by an Ontario Graduate Scholarship and a Doctoral award from the MRC. D. P. Munoz is a MRC Scientist and EJLB Foundation Fellow.
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FOOTNOTES |
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Address for reprint requests: D. P. Munoz, Dept. of Physiology, Queen's University, Kingston, Ontario K7L 3N6, Canada.
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 23 December 1998; accepted in final form 1 June 1999.
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REFERENCES |
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