JemrJournal of Eye Movement Research1995-8692Bern Open PublishingBern, Switzerland10.16910/jemr.12.1.2Research ArticleEffect of visual attention and horizontal vergence in three-dimensional space on occurrence of optokinetic nystagmusKanariKei1KanekoHirohiko2Tamagawa University, Tokyo,
JapanTokyo Institute of Technology, Kanagawa,
Japan28022019201912110.16910/jemr.12.1.22019Kanari, K., & Kaneko, H.This work is licensed under a Creative Commons Attribution 4.0 International License, ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use and redistribution provided that the original author and source are credited.
OKN corresponding to the motion of the fixating area occurs when a stimulus has two areas separated in depth containing motion in different directions. However, when attention and vergence are separately directed to areas with different motions and depths, it remains unclear which property of attention and vergence is prioritized to initiate OKN. In this study, we investigated whether OKN corresponding to motion in the attending or fixating area occurred when two motions with different directions were presented in the central and peripheral visual fields separated in depth. Results show that OKN corresponding to attended motion occurred when observers maintained vergence on the peripheral stimulus and attended to the central stimulus. However, OKN corresponding to each motion in the attending area and in the fixating area occurred when observers maintained vergence on the central stimulus and attended to the peripheral stimulus. The accuracy rate of the target detection task was the lowest in this condition. These results support the idea that motion in the attended area is essential for occurrence of OKN, and vergence and retinal position affect the strength of attention.
The eyes’ rhythmic movement, known as optokinetic nystagmus (OKN), is
induced when a sustained moving stimulus is presented in the visual
field. OKN consists of a slow phase (pursuit movements in the direction
of stimulus motion) and a fast phase (saccadic return movements opposite
the direction of motion) [1]. OKN serves to stabilize a moving
stimulus’s image on the retina, and it has the following characteristics
related to the stimulus’s physical features. OKN gain (ratio of slow
phase velocity to stimulus velocity) decreases when a stationary object
appears in the plane of the moving stimulus [2]. OKN gain also
decreases as the width or area of the moving stimulus
decreases [3]. Some studies have reported that OKN gain
decreases when the central visual field is occluded [4, 5, 6, 7].
OKN is influenced not only by the stimulus motion at eye position but
also by that at attention position, which can be redirected to another
location, while eye position is maintained in one location [8].
For example, the motion on which the observer focuses elicits OKN when
two patterns moving in different directions are superimposed on the same
depth plane [9], and when a motion parallax stimulus containing
multiple motion areas with different velocities are
presented [10]. Attention paid to motion in the peripheral
visual field facilitates OKN corresponding to that evoked by the motion
when the central visual field-of-motion stimulus is
absent [5, 6]. OKN corresponding to the motion direction of an
attended (refers to the attention instructed by the target detection
task in this study; the same hereinafter.) stimulus occurs when stimuli
moving in different directions are presented in different areas on the
same plane [11]. These studies indicate that OKN corresponding
to attended motion occurs when stimuli are presented in the
two-dimensional plane.
OKN corresponding to a binocularly fused moving stimulus occurs when
motion stimuli are presented in different depth planes. For example,
when stimuli moving in opposite directions were presented in different
depth planes at the central area and its upper and lower areas, OKN
corresponding to the binocularly fused moving stimulus
occurred [12]. Another study showed that OKN gain decreased as
binocular disparity of motion stimulus increased, while vergence was
kept on a vertical line with zero disparity relative to the
display [13]. Attention seems to affect these results, showing
the effect of vergence on OKN because directing vergence to certain
depth should involve, at least partly, voluntarily control. However,
effects of vergence and attention on OKN in three-dimensional space were
not discussed in previous studies.
The results of studies with a two-dimensional stimulus, as shown
above, are presumed to show attention’s influence on OKN because the
influence of vergence is constant all over the stimulus. Assuming that
attention is the essential factor for initiating OKN in
three-dimensional space, the claim in the previous study [12]
that OKN occurred corresponding to motion on the vergence plane
regardless of the central and peripheral visual fields can be
interpreted as the effect of the observer’s attention directed with
vergence. This study aimed to examine the validity of that presumption
by investigating whether OKN corresponding to attended motion occurred
when two movements in different directions were separately presented on
different depth planes in the central and peripheral visual fields while
manipulating vergence distance and attentional state.
Methods
This study presented two motion stimuli in different directions in
the central and peripheral visual fields, separated in depth defined by
binocular disparity. The observer attended to one motion stimulus while
maintaining vergence distance on the anteroposterior axis at the center
of the stimulus, independent of attention location. The observer
responded with a numeral presented randomly and moved with the same
velocity and direction as the random dots in the attended plane. This
task’s purpose was to keep the observer’s attention on the instructed
field of stimulus. We verified the vergence state during the trial by
measuring binocular eye movements and investigated whether OKN occurred
in correspondence to the attention field’s motion or the vergence
distance’s motion.
Participants
One author and six naïve volunteers (six males and one female, aged
23–33 years) participated in this experiment. All had normal or
corrected-to-normal visual acuity. They were verified to have a
stereo-acuity of at least 40 sec of disparity using a stereo-test (The
Fly Stereo-test, Stereo Optical Co., Inc.) and to perceive correctly the
stimulus depth with ±4° of horizontal disparity with respect to the
display plane before the experiment. All observers provided written
informed consent before participating. The study was approved by the
Tokyo Institute of Technology Epidemiological Research Ethics Committee
and conducted in accordance with the Code of Ethics of the World Medical
Association (Declaration of Helsinki).
Materials
Figure 1 displays an example of stimuli. Left and right panels are
for cross fusion, and center and right panels are for parallel fusion.
The stimulus for the left-eye image was drawn in red and viewed through
a red filter; the stimulus for the right-eye image was drawn in blue and
viewed through a blue filter (the anaglyph technique). Background
luminance was 0.01 cd/m2. The motion stimulus consisted of
randomly positioned moving dots, with a size, velocity, and density of
0.8 deg, 31.0 deg/s, and 0.4 dots/deg2, respectively.
Luminance of a red dot for the left eye was 8.1 cd/m2, and of
a blue dot for the right eye was 3.1 cd/m2. The difference in
luminance between dots for the left and right eyes did not affect
stereopsis. Figure 2 illustrates the stimulus schematically. The central
stimulus was circular with a diameter of 13.6 deg and presented at the
display’s center (the circular line shown in Figure 2 here was not
actually presented). The peripheral stimulus was presented in the rest
of the display (36.3 × 27.2 deg). The central stimulus
and the peripheral stimulus were presented simultaneously. Dots in each
stimulus area moved vertically, and areas’ motion directions were always
opposite each other (upward and downward). The reason to use vertical
motion was to facilitate the horizontal binocular fusion to the
stimulus. Because the stimulus had horizontal disparity, the effort for
binocular fusion sometimes produced horizontal eye movement similar to
OKN. One of the two areas was presented on the display plane (visual
distance 57.0 cm), and the other was presented on the plane with 4°
(front) or −4° (behind) of disparity with respect to the display plane,
corresponding to the theoretical distance of 35.6 cm or 143.8 cm,
respectively, when the inter-ocular distance was 6.6 cm. Observers were
instructed to confine their vergence to the plane with 4° or −4° of
disparity. We used such a large disparity because the two different
depth planes were fused when disparity of stimuli was small (Panum’s
fusional area [14, 15]). The target used to maintain attention on
the instructed depth plane was either “0” or “1.” The target’s size,
velocity, direction, and depth were the same as those of the attended
plane’s stimulus dots. Dots and the target of the central and peripheral
areas disappeared at the areas’ borders.
Stimulus configuration used in the
experiment: Left and center panels are for cross fusion, and center and
right panels are for parallel fusion. By means of free-fusing, both
cross and parallel fusers can make an impression on the 3D structure of
the stimulus. The numeral “1” indicates the target (presented near the
center).
Schematic illustration of stimulus: Left
and right panels, respectively, show front and top view of stimuli.
Arrows show direction of motion. Circle (not actually presented) show
border of area where dots were presented. Central and peripheral areas
have different depths.
Procedure
Figure 3 displays the time course of stimuli presentation for one
trial. In one trial, first, the observer was instructed to which plane
to direct attention and vergence. Following the observer’s button press,
a pair of dots—one for the left and one for the right eye—were
presented. Then, the observer fused them to perceive one dot on the
depth plane to which vergence was directed. After the observer fused the
two dots, a button press caused stimuli to appear. The observer attended
to the instructed motion stimulus while maintaining vergence on the
instructed depth plane. During motion stimuli presentation, the observer
directed the eyes to the central area. No fixation point was presented,
and the duration of stimulus presentation was 3.6 s. In a trial, the
target appeared once for 0.8 s in the attended area at randomly decided
timing, 1.6–2.5 s after stimulus onset. Each dot appeared at the edge of
the stimulus motion area and then moved continually to the area’s other
edge. The target disappeared when it exceeded the center circle and the
peripheral area’s boundary. A dot with zero disparity appeared for 2.5 s
after presentation of a test stimulus. Then, the observer fixated the
dot and responded with the target numeral (0 or 1) presented
(subjectively). Response time was unlimited, and the observer received
feedback. After the response, a button press launched the next
trial.
Time course of stimulus presentation in a trial: Left and
center panels are for cross fusion, and center and right panels are for
parallel fusion. By means of free-fusing, both cross and parallel fusers
can make an impression of the 3D structure of the stimulus. The observer
attended to the motion stimulus while maintaining vergence at the
different (or same) depth plane from attended plane on the
anteroposterior axis at the center of stimulus.
Figure 4 illustrates a schematic of experimental conditions, i.e.,
four conditions of vergence and attention: (a) to attend and direct
vergence to the center of the stimulus (Attention Center/Vergence Center
[ACVC], Figure 4a); (b) to attend and direct vergence to the periphery
(Attention Periphery/Vergence Periphery [APVP], Figure 4b); (c) to
attend to the center and to direct vergence to the periphery (Attention
Center/Vergence Periphery [ACVP], Figure 4c); and (d) to attend to the
periphery and to direct vergence to the center (Attention
Periphery/Vergence Center [APVC], Figure 4d). These conditions were
conducted in separate blocks, and their order differed among observers.
Two conditions of vergence (±4°) and two conditions of motion direction
(upward and downward) to which to attend were randomized within one
block. Each condition of attended and vergence plane was repeated three
times for each observer, and each observer took four blocks of different
conditions, completing 48 trials.
Schematic illustration of stimulus in each
condition. All panels show top view. Gray and black squares,
respectively, show depth planes where attention was paid and vergence
was directed. Dotted lines show the plane of display. See texts for the
details.
Apparatus & analysis
Observers sat in a dark room with their heads fixed on a chin rest,
viewing a CRT monitor (GDM F500R, SONY, 1400 × 1050 pixels, 36.3 × 27.2
deg) from a distance of 57 cm. They observed the stimulus while wearing
glasses with a red filter for the left eye and a blue filter for the
right eye. Stimuli were produced and presented using a PC (MacBook Pro,
Apple) and MATLAB (MathWorks) with Psychophysics Toolbox
extensions [16, 17, 18]. Observers responded using a numeric
keyboard.
Binocular eye positions were recorded with an EyeLink CL (SR
Research), a video-based eye tracker, and sampling data with 1000 Hz.
Because it has been reported that the contact lenses slip on the eye
during and before/after blinks [19], the data during that period
is unreliable. Data for 200 ms around eye blinks were excluded from
analysis to reduce the noises due to measurement and blinking itself.
Peaks at the slow phase and fast phases’ transition points were detected
using the “findpeaks” function in MATLAB, which finds local maxima in
the data with some parameters. To find relevant peaks corresponding to
saccades from the data including noise in the system or ocular tremor,
we analyzed the peaks that dropped off on both sides by at least 0.1 deg
relative eye position by setting a parameter of “findpeaks” function.
OKN frequency was calculated by dividing the number of peaks in one
trial by the duration of stimulus presentation (3.6 s). Velocities
before and after the peaks were calculated using data for 50 ms and
compared. Since it has been reported that the velocity of the fast phase
requires no less than 10 deg/s [20], if at least one of the
velocities was no less than 10 deg/s, the peak was defined as the point
of phase transition in an OKN and the faster velocity of the two phases
was defined as a velocity of fast phase. Slow phase velocity was
calculated by averaging each trial’s velocities. Next, gains were
averaged over three repetitive trials under each condition for each
observer. Each OKN’s gain was defined as a ratio of slow phase velocity
to stimulus velocity (31.0 deg/s), and the gain was defined as zero when
the OKN frequency in the trial was zero. Gains corresponding to motion
in attended and non-attended fields were calculated separately.
Horizontal vergence was obtained from the two eyes’ visual direction.
The interocular distance was assumed to be 6.6 cm. On the basis of the
vergence angle to the display distance (6.64°), positive and negative
vergence angles were defined as convergence and divergence,
respectively.
Results
Figure 5 shows tracings of eye position for two naïve observers
during one trial as examples. Each panel presents: (a) the result of the
ACVC condition (attention and vergence directed to the center); (b) APVP
condition (attention and vergence directed to the periphery); (c) ACVP
condition (attention directed to the center, and vergence to the
periphery); or (d) APVC condition (attention directed to the periphery
and vergence to the center), respectively. In parentheses under the
condition in the figure, the direction of attended motion is noted. The
upper panel’s vertical axis presents the eye’s vertical position (deg),
signed positive in the display’s upper side. The horizontal axis
presents time (ms) from stimulus onset. The lower panel’s vertical axis
presents the vergence angle relative to the display (deg), signed
positive when eyes converged and negative when they diverged. The solid
line shows the disparity of the plane to which eyes were directed, and
the dotted line shows the disparity of the plane to which attention was
directed. Line drawings inserted in each panel’s upper part present the
predicted OKN’s shape, corresponding to the attended motion’s direction
for each motion condition. For example, when observers attended to
upward motion, the eye’s position was predicted to move upward slowly to
pursue the motion of the stimulus and then move quickly downward. The
left two and the right two panels show Observer 1 and Observer 2’s
results, respectively.
Trace of eye position in a trial for two
observers (OB1 and OB2): The upper four panels depict results of
vertical eye position. The lower four panels depict results of
horizontal vergence. The line drawing inserted above each panel presents
a schematic representation of OKN corresponding to the attended motion
in the condition. Horizontal lines in the lower panel show the disparity
of the plane to which vergence was instructed to direct, and dotted
lines show that to which attention was instructed to
direct.
As Figure 5a’s upper panel shows, the eye moved downward slowly to
follow the dots and then moved upward quickly when the observer attended
to the downward motion in the central area and confined vergence to the
same plane. Eye movement was OKN corresponding to the central (attended)
motion. Figure 5a’s lower panel shows that the observer confined
vergence mostly to the plane with −4° of disparity immediately after the
test stimulus was presented, and then vergence shifted slightly to the
plane of display (0° of disparity) when the observer was instructed to
confine vergence to the plane with −4° of disparity. Similarly, in
Figure 5b’s upper panel, the eye moved downward slowly and then moved
back quickly when the observer attended to the downward motion in the
peripheral area and confined vergence to the plane. Eye movement was OKN
corresponding to the peripheral (attended) motion. Figure 5b’s lower
panel shows that when the observer confined vergence to the plane with
−4° of disparity, vergence varied around −4° of disparity. These OKN
results follow those of previous studies [11, 12].
Similarly, in Figure 5c’s upper panel, the eye moved up slowly and
then moved down quickly when the observer attended to the upward motion
in the central area and confined vergence to the plane of different
depth in the peripheral area. Eye movement was OKN corresponding to the
attended motion. Figure 5c’s lower panel shows that when the observer
was instructed to confine vergence to the plane with 4° of disparity,
the observer confined vergence to a position of about 8° of disparity
immediately after the test stimulus was presented, and then, with time,
vergence shifted to the plane with 4° of disparity. In Figure 5d’s upper
panel, however, the eye sometimes moved down slowly and then moved up
quickly (the first and third arrows in Figure 5d) when the observer
attended the upward motion in the peripheral area and confined vergence
to the plane of different depth in the central area. Eye movement was
OKN corresponding to motion in the plane to which vergence was confined.
Conversely, OKN corresponding to the attended motion also occurred (the
second and forth arrows in Figure 5d). In Figure 5d’s lower panel, when
the observer was instructed to confine vergence to the plane with −4° of
disparity, the observer did so, to a position around −4° of disparity
immediately after test stimulus presentation, and then, vergence shifted
to a position of about −2° of disparity.
To clarify the results’ trend, we calculated OKN frequencies
corresponding to motion directions of attended and non-attended planes
for each trial. In Figure 5a’s
upper panel, for example, the attended motion’s direction was
downward, and nystagmus corresponding to the motion occurred 12 times
during a trial. We calculated the frequency of OKN for 1 sec and used
that as an index, i.e., 3.33 Hz (12/3.6 s). Conversely, the non-attended
motion’s direction was upward, and corresponding nystagmus did not
occur. Therefore, the OKN frequency was 0. Averaged OKN frequencies for
vergence 4° condition in ACVC, APVP, ACVP, and APVC were 2.407 (0.406),
1.310 (0.406), 1.184 (0.364), and 0.245 (0.164), respectively (the value
in parentheses shows standard deviation). Similarly, averaged OKN
frequencies for vergence −4° condition were 2.037 (0.682), 1.296
(0.536), 0.853 (0.406), and 0.311 (0.221). Averaged OKN frequencies for
the upward condition were 1.872 (0.554), 1.303 (0.720), 0.926 (0.518),
and 0.238 (0.286). Averaged OKN frequencies for the downward condition
were 2.573 (0.606), 1.303 (0.413), 1.111 (0.541), and 0.317 (0.120). For
all conditions, results of different depths (±4°) and of motion
directions (upward and downward) were averaged because the OKN frequency
did not significantly differ for different depths (main effects of
condition; F(3,18) = 32.262,
p < .001, main effects of depth ;
F(1,6) = 2.612, p > .10,
interaction of condition vs. depth;
F(3,18) = 1.903, p > .10), and
motion directions (main effects of condition;
F(3,18) = 32.262, p < .001, main
effects of direction ; F(1,6) = 1.116,
p > .10, interaction of condition
vs. direction; F(3,18) = 3.107,
p > .05) for each observer. Averaged results across
observers are shown in Figure 6. Each panel presents the result for each
combination of conditions of vergence and attended plane as shown in
Figure 4. The horizontal axis presents the position of stimulus motion
and of instructed vergence and attention in parentheses. The vertical
axis presents OKN frequency corresponding to each area’s motion. Error
bars show ± SEM.
Mean frequency of OKN in the experiment for each condition
of directed vergence and attention: The horizontal axis presents the
position of stimulus motion to which OKN corresponded, and the
parentheses under that indicate instruction for observers. The vertical
axis presents the frequency of OKN corresponding to the motion of each
area. Error bars show ± 1 SEM.
The result in Figure 6a clearly shows that OKN frequency
corresponding to central motion was significantly higher than that
corresponding to peripheral motion when both attention and vergence were
directed to the central area (F(1,6) = 129.380,
p < .001). This result was expected due to results
from previous studies. Similarly, the result in Figure 6b shows that OKN
frequency corresponding to peripheral motion was significantly higher
than that corresponding to central motion when both attention and
vergence were directed to the peripheral area (F(1,6) =
25.032, p < .005). The result in Figure 6c shows
that OKN frequency corresponding to central
motion was significantly higher than that corresponding to peripheral
motion when attention was directed to the central area and vergence was
directed to the peripheral area’s depth plane (F(1,6) =
29.841, p < .005). The result in Figure 6d shows,
however, that OKN frequency corresponding to peripheral motion and to
central motion did not significantly differ when attention was directed
to the peripheral area and vergence to the central area
( F(1,6) = 1.404, p > .10).
To verify the significance of results of OKN frequency corresponding
to the attended motion mentioned above, a one-way ANOVA was performed on
data for the four conditions. The main effect of
condition was significant for frequency
( F(3,18) = 32.262, p < .001).
Multiple comparison tests using Ryan’s method (α = 0.05) showed that
differences between any combinations of results were significant, except
for that between results of the APVP and the ACVP conditions
( p > .10). As with analytical results on OKN
frequency, we calculated the OKN gain corresponding to attended motion
and non-attended motion in each trial. For example, in Figure 5c’s upper
panel, the direction of non-attended motion was downward, and
corresponding nystagmus did not occur. Therefore, the OKN gain
corresponding to non-attended motion in this trial was 0. Conversely,
the direction of attended motion was upward, and corresponding nystagmus
occurred six times. Therefore, the average gain across six OKNs, 0.22,
was used as the OKN gain corresponding to this trial’s attended motion.
Averaged OKN gains for vergence 4° condition in ACVC, APVP, ACVP, and
APVC were 0.416 (0.165), 0.400 (0.244), 0.258 (0.088), and 0.158
(0.128), respectively (the value in parentheses shows standard
deviation). Similarly, averaged OKN gains for vergence −4° condition
were 0.425 (0.231), 0.403 (0.176), 0.198 (0.128), and 0.164 (0.120).
Averaged OKN gains for the upward condition were 0.395 (0.196), 0.3424
(0.266), 0.224 (0.118), and 0.194 (0.201). Averaged OKN gains for the
downward condition were 0.459 (0.274), 0.379 (0.206), 0.232 (0.118), and
0.127 (0.065). Results of different depths (± 4°) and motion directions
(upward and downward) were averaged in each condition because the OKN
gain did not differ significantly for different depths (main effects of
condition; F(3,18) = 9.388,
p < .001, main effects of depth ;
F(1,6) = 0.509, p > .10,
interaction of condition vs. depth;
F(3,18) = 0.678, p > .10) and
motion directions (main effects of condition;
F(3,18) = 9.404, p < .001, main
effects of direction ; F(1,6) = 0.025,
p > .10, interaction of condition
vs. direction; F(3,18) = 0.845,
p > .10) in each condition. Average results of gain
across observers are shown in Figure 7. The horizontal axis is the same
as in Figure 6. The vertical axis shows the gain (slow phase
velocity/stimulus velocity) of OKN corresponding to motion of the
central or peripheral areas. Error bars show ± SEM. The result in Figure
7a shows that the OKN gain corresponding to central motion was
significantly higher than that corresponding to peripheral motion when
both attention and vergence were directed to the central area
( F(1,6) = 27.134, p < .005). The
result in Figure 7b shows that OKN gain corresponding to peripheral
motion was significantly higher than that corresponding to central
motion when both attention and vergence were directed to the peripheral
area (F(1,6) = 17.588, p < .01),
although motion in the opposite direction was presented in the central
area. These results are consistent with previous studies and
qualitatively consistent with present frequency results (Figures 6a and
6b). The result in Figure 7c shows that OKN gain corresponding to
central motion was significantly higher than that corresponding to
peripheral motion when attention was directed to the center area and
vergence was directed to the peripheral area (F(1,6) =
11.851, p < .05). The result in Figure 7d shows that
OKN gain corresponding to peripheral motion did not significantly differ
from that corresponding to central motion when attention was directed to
the peripheral area and vergence was directed to the central area
( F(1,6) = 0.364, p > .10). These
results are also qualitatively consistent with frequency results
(Figures 6c and 6d).
Mean gain of OKN in the experiment for
each condition of vergence and attention instructed to direct: The
vertical axis presents the gain of OKN corresponding to the motion of
each area. Other aspects of the figure are the same as those in Fig
6.
To verify the significance of results of OKN gain corresponding to
the attended motion mentioned above, a one-way ANOVA was performed on
data for the four conditions. As a result, the main effect of
condition was significant for frequency
( F(3,18) = 9.404, p < .001).
Multiple comparison tests using Ryan’s method (α = 0.05) showed that
differences between any combination of results were significant, except
for the combination in which attention and vergence were directed to the
same plane (Figures 6a and 6b) and that in which attention and vergence
were directed to different planes (Figures 6c and 6d)
( p > .10).
Mean results of the vergence angle (deg) and percentage of correct
answers for the target detection task (%) in each condition are shown in
Table 1. The mean percentage of keeping vergence within ±1 deg of the
instructed plane during a trial in conditions of ACVC, APVP, ACVP, and
APVC were 38.0 (17.7), 29.6 (18.9), 22.7 (12.2) and 30.3 (14.6) %,
respectively (the value in parentheses shows standard deviation). In the
table, we also present results of a paired t-test to verify whether the
mean vergence angle when confining vergence to 4° and −4° of disparity
differed significantly from theoretical values of 4° and −4°
respectively. As a result, in all conditions, the mean vergence angle
when confining vergence to 4° of disparity (cross disparity) did not
differ significantly from the theoretical value of 4°; however, the mean
vergence angle when confining vergence to −4° of disparity (uncrossed
disparity) did significantly differ from the theoretical value of −4°.
This result indicates that the mean vergence to −4° of disparity was not
directed to the instructed vergence plane. To test for significance in
differences of mean vergence angle in each condition when instructed to
direct vergence to −4° of disparity, a one-way ANOVA was performed. The
main effect of condition was not significant for mean
vergence angle (F(3,18) = 0.796, p
> .50). Therefore, we suppose the reason for the difference in the
results of OKN frequency and gain in these conditions was caused by
directing attention and not by the difference in vergence angle.
Mean vergence angle, a paired t-test, and accuracy of target
detection task in each condition.
ACVC
APVP
ACVP
APVC
(a) Vergence condition
4°
−4°
4°
−4°
4°
−4°
4°
−4°
(b) Mean angle of vergence (SE)
3.96° (0.51)
−2.35° (0.34)
4.49° (0.65)
−2.85° (0.19)
4.42° (0.63)
−2.34° (0.21)
4.25° (0.11)
−2.71° (0.48)
(c) p value (t-test): (a) vs
(b)
0.95
0.029*
0.48
0.001*
0.52
0.000*
0.068
0.038*
(d) Percent correct (SE)
66.6% (7.7)
69.6% (4.5)
70.2% (4.7)
45.2% (5.0)
ACVC condition (attention and vergence directed to the center);
APVP condition (attention and vergence directed to the periphery); ACVP
condition (attention directed to the center, and vergence to the
periphery); APVC condition (attention directed to the periphery and
vergence to the center).
Mean correct-answer rates to the target detection task in conditions
of attended and vergence plane, ACVC, APVP, ACVP, and APVC (Figures 4a,
4b, 4c, and 4d) were 66.6%, 69.6%, 70.2%, and 45.2%, respectively. The
correct-answer rate was about 66% in the ACVC condition, which indicates
that this task sufficient for participants to maintain their attention
until the target was detected. To test for significance in differences
of correct-answer mean rates in each condition, a one-way ANOVA was
performed. The main effect of condition was significant
for mean rates of correct answer (F(3,18) = 4.845,
p < .05). Multiple comparison tests using Ryan’s
method (α = 0.05) showed that differences between the value in APVC
(attention directed to the peripheral area and vergence to the central
area) and the value in other conditions differed significantly
( p < .05).
Discussion
In this study, we examined the more essential factors of motion for
generating OKN, retinal location, vergence location, or attentional
location. For this purpose, we investigated OKN properties when two
motions with different directions were presented in central and
peripheral visual fields and on different depth planes, while separately
manipulating vergence and attention direction. As a result, OKN
corresponding to attended motion occurred when the plane of attended
motion was the same as the plane of vergence, no matter whether motion
was presented in the periphery or the center. This result indicates that
retinal location is not essential for generating OKN and is consistent
with the previous study [12]. In the condition with attention
directed to the center and vergence to the plane of periphery, OKN
corresponding to attended motion mainly occurred. However, in the
condition with attention directed to the periphery and vergence to the
center, OKN corresponding to the motion of the attended plane and of the
vergence plane occurred equally. These results indicate that attention
is always necessary for OKN’s occurrence but vergence is not necessarily
important for OKN’s occurrence.
Analysis of the relationship between the vergence position and OKN
frequency indicates that motion in the vergence plane is not essential
for OKN to occur. In the condition that the plane of attention was
consistent with the plane of vergence, observers exactly confined
vergence on the instructed plane when the stimulus had crossed disparity
(front), while observers confined vergence in front of the instructed
plane when the stimulus had uncrossed disparity (behind). However, OKN
frequencies and gains in these conditions did not differ significantly.
In addition, in conditions in which attention and vergence were directed
to different planes, OKNs corresponding to the attended plane’s motion
occurred, but those corresponding to motion on the vergence plane were
much less or about the same. These results indicate that vergence is not
an essential factor for OKN’s occurrence.
From the present experiment’s results, we presume that attention is
the essential factor in producing OKN when motions with different
directions are presented at different depths. This is indicated because
many OKNs corresponding to attended motion occurred in the ACVP
condition (attention directed to the center and vergence to the
periphery) (Figure 4c) and in conditions of ACVC and APVP (Figures 4a
and 4b). The results that OKN frequency and gain corresponding to
attended motion and to motion on the vergence plane did not differ
significantly in the APVC condition (attention directed to the periphery
and vergence to the center) (Figure 4d) might indicate the importance of
motion on the plane of vergence for OKN. However, the accuracy rate of
target detection tasks in this condition was much lower (45.2%) than
those in other conditions (66.6%, 69.6%, and 70.2%). These results
indicate that the magnitude of attention directed to the instructed
plane in the APVC condition was weaker than in other conditions. The
target detection rates in this condition were likely hindered by the
lack of robust OKN. As shown in Figure 5, vergence shifted from the
vergence plane to the target plane during a trial. This fact indicates
that attention and vergence were not completely separated. Therefore, it
would be possible to suppose that the target detection rate was low
because the occurrence of OKN decreased and the image of a target was
not stabilized on the retina properly.
Results below are also consistent with attention’s magnitude being
essential for OKN frequency and gain. OKN gains corresponding to
attended motion were lower in conditions in which attended and vergence
planes differed than in conditions in which they were the same. This is
presumed a decrease in the magnitude of attention to the attended plane
due to attention remaining on the plane of vergence. In the previous
study, OKN corresponding to motion of the central area occurred when
observers confined vergence to the peripheral area [12],
although this hardly occurred in this study (Figure 6b). We suppose the
reason for the difference is the target detection task’s existence. We
also suppose that OKN corresponding to the central motion occurred in
the previous study [12] because observers’ attention remained in
the central area as well as in the peripheral area. Moreover, OKN
corresponding to central motion did not occur in the present study
because the target detection task caused steady, focused attention on
peripheral motion.
However, we did not deny the possibility that stimulus features have
direct effects on OKN frequency and gain. In some conditions, a
difference appeared in OKN frequency and gain, but no difference in the
target detection task’s accuracy rate, thus indicating this presumption.
For example, in conditions ACVC and APVP (attention and vergence
directed to the same plane), no significant difference appeared in the
target detection task’s accuracy rate although significant difference
appeared in OKN frequency. In addition, in conditions in which attended
and vergence plane were inconsistent, OKN gains were lower than in
conditions in which attended and vergence plane were consistent. As
mentioned in the previous study [13], the reason for the
difference is linkage between the optokinetic system and the
stereoscopic system. The OKN gain in animals with stereoscopic vision
was higher than those without it because the stereoscopic signal routed
through the visual cortex supplements direct inputs from the retina to
the pretectum [21, 22, 23]. The OKN gain would decrease in conditions
in which attended and vergence plane were inconsistent because
supplemental cortical inputs to subcortical mechanisms controlling OKN
decreased due to the diplopic image of attended motion.
Attention can be voluntarily separated from the position of the gaze
and vergence although attention is normally linked to them. However,
their connection to attention is enhanced by gazing and directing
vergence together. In such a case, observers have difficulty directing
attention to a different position and depth from the point of gaze and
vergence. OKN corresponding to attended motion occurred when motion
stimuli with different directions were presented at central and
peripheral visual fields on a planar surface [11] or when
attention was directed to the central field and vergence was directed to
the peripheral plane at a different depth from the center. However, OKNs
corresponding to the attended motion were weak in the APVC condition,
probably due to the decrease in attentional magnitude to the peripheral
area because central vision and binocular fusing were not combined. In
summary, separating attention from the central area is not difficult,
but separating attention from a binocularly fused image on the central
area is quite difficult. Certainly, since physical factors such as
stimulus velocity, size, and motion direction (orthogonal directions)
are related to OKN [5], the relationship between these and
attention should also be considered and such an investigation is
needed.
Conclusion
In this study, we investigated whether OKN corresponding to attended
motion occurred when two motions in different directions were presented
in central and peripheral visual fields separated by depth. As a result,
in conditions in which attention and vergence were directed to the same
plane, OKN corresponding to motion on the plane of attention and
vergence occurred regardless of the motion’s presentation position. In
the ACVP condition (attention directed to the center and vergence to the
periphery), OKN corresponding to the attended motion occurred. In the
APVC condition (attention directed to the periphery and vergence to the
center), however, OKNs corresponding to motions on the attention plane
and on the vergence plane occurred. Analysis of horizontal vergence and
the target detection task’s accuracy rate during the trial indicated
that the motion of the attended position, rather than that of the
vergence position or that on the central visual field, is essential for
occurrence of OKN. The relationship between OKN frequency and gain and
the accuracy rate of target detection task during the trial is
consistent with the idea that magnitude of attention is essential for
properties of OKN.
Recently, several reports have demonstrated that visual attention
relates to pupillary light reflex [24, 25, 26],
micro-saccades [27, 28], and vergence eye
movements [29, 30]. We suppose it possible to predict the
directed area of attention based on OKN direction when areas of motion
have different directions in the visual field. By using this method to
predict attentional location in a visual stimulus with various
directions of motion from OKN, it would be possible to know the location
to which a driver is attending (to up or down) in the optical flow, for
example. In addition, predicting attentional state and position more
accurately by combining knowledge from the present study and previous
studies’ findings would be possible. To realize such a system, we need
to ascertain the relationship between attention and OKN, pupillary
response, micro-saccades and other eye movements in more complex
situations in real scenes.
Ethics and Conflict of Interest
The authors declare that the contents of the article are in agreement
with the ethics described in
http://biblio.unibe.ch/portale/elibrary/BOP/jemr/ethics.html
and that there is no conflict of interest regarding the publication of
this paper.
Acknowledgements
We appreciate the volunteers for participating in this study and
anonymous reviewers for their valuable comments and suggestions, which
improved the quality of the paper.
Barnes, G. R., & Crombie, J. W. ( 1985). The interaction of conflicting retinal motion stimuli in oculomotor control.Experimental Brain Research, 59, 548– 558. 10.1007/bf0026134610.1007/BF0026134640293270014-4819Binda, P., Pereverzeva, M., & Murray, S. O. ( 2013). Attention to bright surfaces enhances the pupillary light reflex.The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 33, 2199–2204. 10.1523/JNEUROSCI.3440-12.2013233652550270-6474Brainard, D. H., & Vision, S. ( 1997). The psychophysics toolbox.Spatial Vision, 10, 433–436. 10.1163/156856897x0035710.1163/156856897X0035791769520169-1015Carpenter, R. H. S. ( Ed.)
. ( 1991). Eye movements. CRC Press.
Chauhan, A., & Radke, C. J. ( 2001). Modeling the vertical motion of a soft contact lens.Current Eye Research, 22, 102–108. 10.1076/ceyr.22.2.102.5521114023870271-3683Cheng, M., & Outerbridge, J. S. (1975).Optokinetic nystagmus during selective retinal stimulation.Experimental Brain Research,23,129– 139.10.1007/bf0023545510.1007/BF0023545511835000014-4819Crone, R. A., & Leuridan, O. M. A. (1973).Tolerance for aniseikonia. I. Diplopia thresholds in the vertical and horizontal meridians of the visual field.Albrecht von Graefes Archiv fur Klinische und Experimentelle Ophthalmologie,188,1–16.10.1007/bf0041086010.1007/BF0041086045423550065-6100Dichgans, J. (1977).Optokinetic nystagmus as dependent on the retinal periphery via the vestibular nucleus. Control of Gaze by Brain Stem Neurons.Developmental Neuroscience,1,261– 267.0378-5866Dubois, M. F. W., & Collewijn,H. (1979).Optokinetic reactions in man elicited by localized retinal motion stimuli.Vision Research,19,1105– 1115.10.1016/0042-6989(79)90005-15505680042-6989Engbert,R., & Kliegl,R. (2003).Microsaccades uncover the orientation of covert attention.Vision Research,43,1035–1045.10.1016/s0042-6989(03)00084-110.1016/S0042-6989(03)00084-1126762460042-6989Gresty,M., & Halmagyi,M. (1979).Following eye movements on the absence of central vision.Acta Oto-Laryngologica,87,477–483.10.3109/000164879091264554635200001-6489Hafed,Z. M., & Clark,J. J. (2002).Microsaccades as an overt measure of covert attention shifts.Vision Research,42,2533–2545.10.1016/s0042-6989(02)00263-810.1016/S0042-6989(02)00263-8124458470042-6989Hoffmann,K. P. (1982).Cortical versus subcortical contributions to the optokinetic reflex in the cat. Functional basis of ocular motility disorders, 303-310.Hoffmann,K. P., & Distler,C. (1986).The role of direction selective cells in the nucleus of the optic tract of cat and monkey during optokinetic nystagmus. Adaptive processes in visual and oculomotor systems, 57, 261-266.Howard,I. P., & Gonzalez,E. G. (1987).Human optokinetic nystagmus in response to moving binocularly disparate stimuli.Vision Research,27,1807–1816.10.1016/0042-6989(87)90109-x10.1016/0042-6989(87)90109-X34454700042-6989Howard,I. P., & Simpson,W. A. (1989).Human optokinetic nystagmus is linked to the stereoscopic system.Experimental Brain Research,78,309–314.10.1007/bf0022890210.1007/BF0022890225990400014-4819Kanari,K.,Sakamoto,K., & Kaneko,H. (2017).Effect of visual attention on the properties of optokinetic nystagmus.PLoS One,12,e0175453.10.1371/journal.pone.0175453283886681932-6203Kleiner,M.,Brainard,D.,Pelli,D.,Ingling,A.,Murray,R., & Broussard,C. (2007).What’s new in Psychtoolbox-3.Perception,36,1.0301-0066Mathôt,S.,van der Linden,L.,Grainger,J., & Vitu,F. (2013).The pupillary light response reveals the focus of covert visual attention.PLoS One,8,e78168.10.1371/journal.pone.0078168242051441932-6203Mestre,D. R., & Masson,G. S. (1997).Ocular responses to motion parallax stimuli: The role of perceptual and attentional factors.Vision Research,37,1627–1641.10.1016/s0042-6989(96)00314-810.1016/S0042-6989(96)00314-892312290042-6989Mitchell,D. E. (1966).Retinal disparity and diplopia.Vision Research,6,441–451.10.1016/0042-6989(66)90052-660033730042-6989Montarolo,P. G.,Precht,W., & Strata,P. (1981).Functional organization of the mechanisms subserving the optokinetic nystagmus in the cat.Neuroscience,6,231–246.10.1016/0306-4522(81)90059-272197150306-4522Naber,M.,Alvarez,G. A., & Nakayama,K. (2013).Tracking the allocation of attention using human pupillary oscillations.Frontiers in Psychology,4,919.10.3389/fpsyg.2013.00919243689041664-1078Niemann,T.,Ilg,U. J., & Hoffmann,K. P. (1994).Eye movements elicited by transparent stimuli.Experimental Brain Research,98,314–322.10.1007/bf0022841910.1007/BF0022841980505160014-4819Pelli,D. G. (1997).The VideoToolbox software for visual psychophysics: Transforming numbers into movies.Spatial Vision,10,437–442.10.1163/156856897x0036610.1163/156856897X0036691769530169-1015Posner,M. I. (1978).Chronometric explorations of mind.Lawrence Erlbaum.
Solé Puig,M.,Pérez Zapata,L.,Aznar-Casanova,J. A., & Supèr,H. (2013a). A role of eye vergence in covert attention.PLoS One,8,e52955.10.1371/journal.pone.0052955233828271932-6203Solé Puig,M.,Puigcerver,L.,Aznar-Casanova,J. A., & Supèr,H. (2013b). Difference in visual processing assessed by eye vergence movements.PLoS One,8,e72041.10.1371/journal.pone.0072041240691401932-6203Tamminga,E. P. (1983).Human fixation and voluntary pursuit: the interaction between central and peripheral motion stimuli. Ph.D. thesis, Erasmus University Rotterdam.
van Die,G., & Collewijn,H. (1982).Optokinetic nystagmus in man. Role of central and peripheral retina and occurrence of asymmetries.Human Neurobiology,1,111–119.10.1016/0166-4328(83)90114-671857850721-9075