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Eye-gaze information input based on pupillary response to visual stimulus with luminance modulation

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This study develops an information-input interface in which a visual stimulus targeted by a user’s eye gaze is identified based on the pupillary light reflex to periodic luminance modulations of the object. Experiment 1 examines how pupil size changes in response to periodic luminance modulation of visual stimuli, and the results are used to develop an algorithm for information input. Experiment 2a examines the effectiveness of interfaces with two objects. The results demonstrate that 98% accurate identification of the gaze targeted object is possible if the luminance modulation frequencies of two objects differ by at least 0.12 Hz. Experiment 2b examines the accuracy of a gaze directed information input method based on a keyboard configuration with twelve responses. The results reveal that keyboard input is possible with an average accuracy of 85% for luminance modulation frequencies from 0.75 to 2.75 Hz. The proposed pupillometry based information-input interface offers several advantages, such as low burden on users, minimal invasiveness, no need for training or experience, high theoretical validity, and no need for calibration. Thus, the pupillometry method presented herein has advantages for practical use without requiring the eye’s position to be calibrated. Additionally, this method has a potential for the design of interfaces that allow patients with severely limited motor function to communicate with others.
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RESEARCH ARTICLE
Eye-gaze information input based on pupillary
response to visual stimulus with luminance
modulation
Yumiko MutoID
1,2¤
*, Hideka Miyoshi
1
, Hirohiko Kaneko
1
*
1Dept. of Information and Communications Engineering, Tokyo institute of Technology, Yokohama,
Kanagawa, Japan, 2Brain Science Institute, Tamagawa university, Tokyo, Japan
¤Current address: Brain Science Institute, Tamagawa university, Tokyo, Japan
*muto@lab.tamagawa.ac.jp (YM); kaneko.h.ab@m.titech.ac.jp (HK)
Abstract
This study develops an information-input interface in which a visual stimulus targeted by a
user’s eye gaze is identified based on the pupillary light reflex to periodic luminance modula-
tions of the object. Experiment 1 examines how pupil size changes in response to periodic
luminance modulation of visual stimuli, and the results are used to develop an algorithm for
information input. Experiment 2a examines the effectiveness of interfaces with two objects.
The results demonstrate that 98% accurate identification of the gaze targeted object is pos-
sible if the luminance modulation frequencies of two objects differ by at least 0.12 Hz. Exper-
iment 2b examines the accuracy of a gaze directed information input method based on a
keyboard configuration with twelve responses. The results reveal that keyboard input is pos-
sible with an average accuracy of 85% for luminance modulation frequencies from 0.75 to
2.75 Hz. The proposed pupillometry based information-input interface offers several advan-
tages, such as low burden on users, minimal invasiveness, no need for training or experi-
ence, high theoretical validity, and no need for calibration. Thus, the pupillometry method
presented herein has advantages for practical use without requiring the eye’s position to
be calibrated. Additionally, this method has a potential for the design of interfaces that allow
patients with severely limited motor function to communicate with others.
Introduction
To regulate the amount of light entering the eye, the pupil diameter changes as a function of
the brightness of the object being viewed [1] [2] [3] [4], and the characteristics of this pupillary
light reflex (PLR) have been explored in many studies [e.g., [5] [6] [7] [8]]. The present study
develops an information-input interface in which a visual object targeted by the user’s eye gaze
is detected based on the pupillary light reflex to periodic luminance modulations of the object.
In addition to conventional information-input devices such as the keyboard and mouse, sev-
eral methods have been proposed that use biological signals such as eye-gaze position and
brain waves [see, e.g., [9] [10]]. Unfortunately, the signals produced by such methods have
PLOS ONE | https://doi.org/10.1371/journal.pone.0226991 January 9, 2020 1 / 18
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OPEN ACCESS
Citation: Muto Y, Miyoshi H, Kaneko H (2020) Eye-
gaze information input based on pupillary response
to visual stimulus with luminance modulation.
PLoS ONE 15(1): e0226991. https://doi.org/
10.1371/journal.pone.0226991
Editor: Yoko Hoshi, Preeminent Medical Phonics
Education & Research Center, Hamamatsu
University School of Medicine, JAPAN
Received: April 30, 2019
Accepted: December 10, 2019
Published: January 9, 2020
Copyright: ©2020 Muto et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: We have uploaded
the data underlying the findings described in our
manuscript to GitHub (https://github.com/Yumiko-
data/data.git) as possible as we can.
Funding: This research was supported by
Adaptable and Seamless Technology transfer
Program through Target-driven R&D (A-STEP)
from Japan Science and Technology Agency (JST).
Competing interests: The authors have declared
that no competing interests exist.
some disadvantages for the intended purpose: The brain-wave techniques generally require
a contact sensor, which is extremely expensive and complicated signal analysis to extract the
desired information. Conventional eye-gaze input methods require not only user training but
also calibration to relate the signal from the device to eye position. In addition, even if individ-
ual adjustments are made beforehand, measurements of eye position are not possible in some
cases. In contrast, pupillometry offers various advantages for information input. To begin, it
requires only a relatively inexpensive noncontact sensor. In addition, pupillary response to
light is sufficiently stable and not only requires no calibration to relate the signal to the change
in light intensity, but also requires no user training to improve signal stability. Accordingly,
pupillometry is a promising technique for information input, especially for patients with
extremely limited motor functions, such as those suffering from the locked-in syndrome.
To communicate intentions and as an information-input interface, particularly among
the patients with extremely limited motor function, a method has been proposed that uses the
pupillary response to a cognitive load, such as two-digit mental arithmetic [11]. This method
is used mainly for patients with locked-in syndrome. The study posed yes-no questions and
obtained approximately 3.6 selections per minute with 90% accuracy for healthy participants
and approximately 2.7 selections per minute with 70% accuracy for patients with severe motor
disabilities. However, this accuracy and response frequency are insufficient for practical use,
and the technique subjects the patients to an excessive cognitive load. Recently, Matho
ˆt et al.
[12] proposed an information-input method to estimate the position of covert visual attention
foci that employed pupillometry and that uses visual stimuli consisting of two circles of black
and white that flash alternately. Participants selected a letter by looking at it covertly. The let-
ters were shown within circles with oscillating brightness. Small changes in pupil size reflected
changes in the luminance of the attended stimulus [13], which enabled the stimulus selected
by the participant to be identified in real time independently of eye movement. This algorithm
was based on the finding that PLR could be modulated via covert attention [14] [15] and used
as a communication method by patients with complete loss of motor control. However, multi-
ple numbers and characters must be displayed simultaneously if it is to be used for actual
human–computer interaction (HCI) applications simultaneously. Fundamentally, this
method is based on two response options; for example, selecting one character out of eight
requires repeating three times the process of selection between two patterns, which requires
an excessively long time for information input, making for an inefficient information-input
technique. For use in real-life situations, multiple numbers and characters must be displayed
simultaneously.
Herein, we propose a method to determine gaze direction based on the frequency of the
PLR response to periodic luminance modulations of various visual stimuli. The visual stimulus
consists of circles whose luminance is modulated at various frequencies and that demark
pieces of input information (numerals or characters). Specifically, the user may be presented
with multiple pieces of input information; for example, the numerals 0 to 9. Each numeral is
demarked by a circle whose luminance is modulated at a unique frequency (i.e., a frequency
that differs from that of the circles around the other nine numerals). As the observer gazes at a
circle, the frequency of pupillary oscillation is measured, which allows the item with the same
luminance-modulation frequency to be identified as the target of the gaze. This approach
determines a unique target of the gaze based only on the pupil data and without directly mea-
suring eye gaze. It can be used with multiple simultaneous stimuli that correspond to various
numbers and characters. Previous research used square- or sine-wave-modulated luminance
to explore the pupillary response to visual stimuli and clarify its basic characteristics in order
to understand the mechanisms and construct a PLR model [see, e.g., [16] [17] [18] [19] [20]].
However, it remains unclear how the pupil responds to visual stimuli consisting of multiple
Eye-gaze information input based on pupillary response
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circles whose luminance is modulated at different frequencies. In addition, no reports exist of
the PLR applied to an information-input interface based on items whose luminance is modu-
lated at different frequencies.
This study consists of two parts: First, we investigate the basic characteristics of pupillary
response to a periodic luminance modulation (Experiment 1). Second, we propose an algo-
rithm for a communication system that uses pupillometry and show its effectiveness when
applied to an information-input interface in which multiple visual items are presented simulta-
neously (Experiment 2). As shown in Fig 1, experiment 2a proposes an interface with two
response options (yes or no) and experiment 2b proposes an interface in the form of a numeric
keypad with twelve response options. Experiment 1 presents a single circular visual stimulus
in the center of a screen and modulates its luminance for each trial at one of the following fre-
quencies: 0.25, 0.5, 0.75, 1.0, 1.25, 1.5, 1.75, 2.0, 2.25, 2.5, 2.75 or 3.0 Hz (Fig 1a). The time-
domain pupil-diameter data are analyzed by using a discrete Fourier transform (DFT) to
quantify the characteristics of the pupil response to the luminance-modulation frequency.
This allows us to identify a suitable range of luminance-modulation frequency and to propose
an algorithm to estimate the luminance-modulation frequency of the gaze-targeted item based
only on the pupil data gathered while the patient gazes at the input interface. Experiment 2
applies the algorithm developed in experiment 1. Experiment 2a allows us to evaluate the effec-
tiveness of an input interface that offers two response options (yes or no) and experiment 2b
does the same but for an interface with 12 response options (numerals or characters). Experi-
ment 2a presents two items on a screen (Fig 1b) and the circle gazed at by the observer is
identified by comparing the measured frequency of pupil-size oscillation with the luminance-
modulation frequency of the various items in the interface. Experiment 2b presents twelve
items (characters or numbers) on a screen (Fig 1c) and uses the same approach to identify
the gaze-targeted item. Herein we evaluate the accuracy of this input identification method.
Fig 1. Visual stimuli for (a) experiment 1, (b) experiment 2a, and (c) experiment 2b.
https://doi.org/10.1371/journal.pone.0226991.g001
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Herein, participants were instructed to pay attention to a visual stimulus while looking at it.
This is referred to as overt attention. Previous studies [11] [12] focused on covert visual atten-
tion and intentionally excluded the need for motor (eye) movement. In contrast, our proposed
system was designed to use overt attention as a source of new input data.
Experiment 1: Basic characteristics of pupillary response to
periodic luminance modulation
Method
1. Participants. Ten observers participated in experiment 1, all of which were students
and staff (nine males and one female, aged 23 to 29) affiliated with the Tokyo Institute of Tech-
nology. All had either normal or corrected to normal vision. The experiment was conducted
with the approval of the Ethics Committee of the Tokyo Institute of Technology. Written
informed consent was obtained from each participant.
2. Apparatus. Participants were seated in a chair in a dark room in front of a CRT moni-
tor positioned at a viewing distance of 50 cm (Sony Corporation, GDM-F400, 1280 ×1024 pix-
els, 19 inch). A head-chin rest was used to fix the head position of each participant. Pupil size
and eye position of the left eye were recorded with an eye-movement measurement system
consisting of infrared illumination and a CCD camera (iRecHS2 system, [21]) with a data-
sampling frequency of 333 Hz.
3. Visual stimuli. The visual stimulus used in the experiment consisted of a 3˚diameter
circle on the gray background (16.4 cd/m
2
) of the screen. The luminance of the circle (y
RGB
)
was modulated as follows:
yRGB ¼Asinð2pftÞ þ 127;ð1Þ
where fis the luminance-modulation frequency [Hz] of the circle and A is the amplitude of
the luminance modulation and is fixed at 128, which is half of the maximum RGB value. The
visual stimuli were generated and controlled by using MATLAB (MathWorks, Inc.) and a
function library (Psychtoolbox-3) installed on a Mac Book Air running OS X Yosemite (Apple
Inc.). The gamma value of the CRT monitor was determined to be 2.8 based on measurements
with a luminance meter (CS-100A Luminance and Color Mete, KONICA MINOLTA, INC.)
and the gamma correction was applied to linear RGB values. The darkest stimulus was 0.99
cd/m
2
and the brightest was 99.4 cd/m
2
.
4. Procedure. The circle was presented in the center of the screen (Fig 1a). The RGB val-
ues of this circle were modulated by a sine function to create a grayscale luminance modula-
tion [see Eq (1)]. Twelve luminance-modulation frequencies were tested: 0.25, 0.5, 0.75, 1.0,
1.25, 1.5, 1.75, 2.0, 2.25, 2.5, 2.75, and 3.0 Hz. The frequencies were selected based on the study
[22], which shows that a temporal series of luminance stimuli could be synchronized with
modulations in pupil size at frequencies up to 3.15 Hz in participants aged from 20 to 30 years.
Each trial began by a signal from the participant, and each stimulus was presented for 10 s.
Each session consisted of 12 trials, each with a different frequency, and with the 12 frequencies
presented in random order. Two sessions were conducted for each participant and no practice
trials were held prior to the experiment. Participants started each trial by pressing a start but-
ton after closing their eyes briefly and resting for what they deemed sufficient time between
each trial. Participants were also instructed to pay attention to the visual stimulus while look-
ing at it.
5. Analysis. The initial second of pupil data was excluded from the analysis because pupil
size is known to be influenced by the onset of visual stimulus [6]. The data were then smoothed
by applying a moving-average filter with the duration of 120 ms, that is each mean is calculated
Eye-gaze information input based on pupillary response
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over a sliding window of length 40 data. After this preprocessing, the frequency characteristics
of the data were explored by applying a DFT [23]. Specifically, the frequency with the highest
power was determined based on the periodogram power spectral density (PSD), which was
estimated from the frequency components obtained from the DFT of the measured and nor-
malized time-domain data of pupil size. The frequency steps in the DFT were approximately
0.01 Hz [24]. A periodogram is a nonparametric method for estimating PSD and is defined
below. Comparative reduction of noise components is an advantage of this technique and
involves squaring the amplitude of the DFT of a sample and scaling it for comparison with
other methods in which a simple spectrum is calculated. Specifically, this is done as follows:
PxxðfÞ ¼ 1
LFsjX
L1
n¼0
xLðnÞej2pfn=Fsj2;ð2Þ
where F
s
is the sampling frequency and P
xx
(f) is the PSD of a signal x
L
(n) with length L. All
calculations were done offline using the Matlab signal processing toolbox (MathWorks, Inc.).
There are two more reasons why we applied the DFT analysis: First, the use of visual stimuli in
which the luminance was sinusoidally modulated led us to expect a similar sinusoidal oscilla-
tion of the pupil diameter. If the DFT reveals a strong frequency component in the sinusoidally
modulated data, this frequency could serve as an appropriate index of synchronization. Sec-
ond, given two or more visual items with different luminance-modulation frequencies (Experi-
ment 2), the influence of items not targeted by the gazed of the patient may be quantified by
comparing the PSD of the luminance-modulation frequencies of these items.
Results and discussion
1. Frequency analysis of pupillary response. In experiment 1, we investigated the time
domain data of pupil response to an isolated visual stimulus presented at the center of a screen
and with one of 12 different luminance-modulation frequencies. Fig 2 shows examples for one
participant of the measured time-domain data for pupil diameter (right column) in response
to the 12 luminance-modulation frequencies (left column). Fig 3 shows the PSD obtained as a
function of frequency by applying a DFT to the data of Fig 2. The red lines indicate the lumi-
nance-modulation frequency for the given visual stimulus.
These results show that, for all luminance-modulation frequencies f, the PSD peak, which
indicates the main frequency at which the pupil size is modulated, is approximately the same
as the luminance-modulation frequency of the gaze-targeted visual stimulus. In other words,
the modulation of pupil size is synchronized with the luminance modulation of the visual stim-
ulus, as expected. However, the magnitude of the PSD peak depends on the luminance-modu-
lation frequency of the visual stimulus. Therefore, to quantify the change in PSD frequency, we
averaged the PSD peak over all the participants for each luminance-modulation frequency (Fig
4). The results show that the PSD peak decreases with increasing luminance-modulation fre-
quency. A nonlinear regression analysis shows that this relationship may be approximated
with high explanatory power by the exponential function
fðxÞ ¼ aexpðbxÞ ð3Þ
Fitting Eq (3) to the data gives a = 3.545, b = 2.844 (R
2
= 0.97, root mean square
error = 0.09). This decrease in PSD peak with increasing frequency is attributed to the funda-
mental characteristics of the pupil response. Numerous previous studies have shown that
the amplitude of pupil-size modulation depends on the luminance modulation frequency
of the visual stimulus. The amplitude of pupil-size modulation is small in response to rapid
luminance modulations[see, e.g., [6]]. Because the PSD analysis applied herein is based on the
Eye-gaze information input based on pupillary response
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amplitude of pupil-size modulations [Eq(2)], the exponential decrease in Fig 4 is attributed to
the differences in PSD amplitude at each frequency. Therefore, a meaningful comparison of
PSD magnitudes in response to luminance-modulation frequencies would require a correction
for the fundamental difference in the pupil response amplitude.
2. Estimation of oscillation frequency f of visual stimulus. This study estimates the
luminance-modulation frequency fof the visual stimulus from the measured oscillations in
pupil size. First, for each trial, we calculated the PSD for each of the 12 frequencies (f= 0.25,
0.5, 0.75, 1.0, 1.25, 1.5, 1.75, 2.0, 2.25, 2.5, 2.75, or 3.0 Hz). Next, the PSD for each frequency
Fig 2. Experiment 1: (a) luminance-modulated visual stimuli and (b) change in pupil size [pix] as a function of
time. The initial second of data is excluded from the analysis. See text for details.
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Fig 3. Experiment 1: Examples of DFT of time-domain pupil-size data; the results are for a single participant. The red line
shows the luminance-modulation frequency of the gaze-targeted visual stimulus.
https://doi.org/10.1371/journal.pone.0226991.g003
Fig 4. Experiment 1: Average PSD of subjects as a function of luminance-modulation frequency of gaze-targeted visual
stimulus.
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was corrected by multiplying by the weight
o¼1
fðxÞ¼1
aexpð bxÞ;ð4Þ
which is the reciprocal of Eq (3), because the PSD varies exponentially with modulation fre-
quency, as shown in Fig 4. We determine the parameters aand bin the exponential function
f(x) [Eq (3)] from a nonlinear regression analysis of the data (see Fig 4). After this correction,
the PSD results for the 12 frequencies are compared to estimate the frequency f0that produces
the largest PSD (PSD
max
). If the estimated frequency f0corresponds to the luminance-modula-
tion frequency fof the gaze-targeted visual stimulus, then the estimate of f0is considered
successful. Table 1 lists the estimation accuracy averaged over the 10 participants for each fre-
quency. An accuracy of 90% or greater is obtained at all frequencies except for 0.5 and 3.0 Hz,
which have accuracies of 80% and 30%, respectively. These results reveal that the proposed
method allows us to estimate the gaze point with high accuracy (90%) if the luminance-modu-
lated frequency of the visual stimulus is between 0.75 and 2.75 Hz. Table 2 is the estimation
confusion matrix. The first column shows the frequency of the estimated stimulus (Hz),
whereas the actual frequency is shown in a horizontal row. Estimation error was highest at 3
Hz, which indicated that 3 Hz was not suitable for application in the system. An upper limit of
2.75 Hz was more appropriate.
Experiment 2: Information-input interface and its evaluation
Method
1. Participants. Experiment 2a used ten male participants aged 22 to 29 years and experi-
ment 2b used eight participants (five males and three females) aged 21 to 28 years, all of whom
Table 1. Experiment 1: Accuracy for each frequency.
Frequency[Hz] 0.25 0.5 0.75 1.0 1.25 1.5 1.75 2.0 2.25 2.5 2.75 3.0
Accuracy[%] 90 80 90 90 90 90 100 90 100 100 100 30
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Table 2. Experiment 1: Confusion matrix.
Estimated frequency [Hz]
0.25 0.5 0.75 1.0 1.25 1.5 1.75 2.0 2.25 2.5 2.75 3.0
Actual frequency [Hz]
0.25 91 0 0 0 0 0 0 0 0 0 0
0.5 0 80 0 0 1 0 0 0 0 0 1
0.75 0 0 9000000001
1 0 0 0 90 0 0 0 0 0 0 1
1.25 0 0 0 0 90000001
1.5 0 0 0 0 0 90 0 0 0 0 1
1.75 0 0 0 0 0 0 10 00000
2 0 0 0 0 0 0 0 90 0 0 1
2.25 0 0 0 0 0 0 0 0 10 0 0 0
2.5 0 0 0 0 0 0 0 0 0 10 0 0
2.75 0 0 0 0 0 0 0 0 0 0 10 0
3 3 0 0 1 0 0 0 0 1 2 0 3
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were students or staff affiliated with the Tokyo Institute of Technology. All participants had
either normal or corrected to normal vision. The two experiments were conducted on different
dates and times. One participant participated in both experiments. The experiments were
approved by the Ethics Committee of the Tokyo Institute of Technology. A written informed
consent was obtained from each study participant.
2. Apparatus and analysis. The apparatus for experiment 2 and its analysis are the same
as for experiment 1.
3. Procedure.
1. Experiment 2a: Communication interface with two response options
This interface is intended to be used for a communication device that accepts only two
answers, such as yes or no. Two circles separated by a 1˚viewing angle appear side by side
on the screen (Fig 1b) and serve as visual stimuli. The left circle is modulated one of the fol-
lowing eight luminance-modulation frequencies: f= 0.75, 1, 1.25, 1.5, 1.75, 2, 2.25, and 2.5
Hz. The luminance-modulation frequency of the right visual stimulus was 0.06, 0.12, or
0.25 Hz higher than that of the left stimulus. For example, when the left circle was modu-
lated at 0.75 Hz, the right circle was modulated at 0.81, 0.87, or 1.0 Hz. In a given experi-
mental session, each combination of stimulus frequencies was presented once, so 3×8 = 24
trials were conducted in total. The luminance-modulation frequencies of the left and right
circles differed by 0.06, 0.12, or 0.25 Hz to determine the smallest possible frequency differ-
ence Δffor which the gaze position of the pupil could be differentiated. We assumed that
this combination of frequencies could be used to examine how the luminance modulation
of the adjacent visual object affects the results. The participants were instructed to direct
their gaze at the left or right circle. We refer to the condition under which eye gaze was
directed at the right (left) circle as the R (L) condition. Each participant took part in two
sessions so that the experiment comprised a total of 48 trials. All of the combinations of sti-
muli and instructions were presented in random order. Each session was divided into two
sets of 12 trials, with each set of trials conducted separately. In each trial, first, a fixation
point was presented at the center of a gray background. After participants pressed the start
button to begin the trial, an “R” or “L” was displayed, instructing the participants to gaze at
either the right or left circle. The luminance of the circles was then modulated for 8 s while
the participants directed their gaze at the designated circle. After closing their eyes to rest as
needed, the participants pressed the start button for the next trial. No training was done in
advance of the experiments.
2. Experiment 2b: Information-input interface with 12 options
This interface is intended to be used as an input device (e.g., a numeral or character key-
board) with a small number of keys. Twelve circles were presented simultaneously on the
screen (see Fig 1c), with a 1˚viewing-angle separation between the edges of adjacent cir-
cles. The luminance-modulation frequencies of the circles were, from left to right, 0.58,
0.70, 0.82 for the top row, 0.94, 1.06, 1.18 for the second row, 1.30, 1.42, 1.54 for the third
row, and 1.66, 1.78, 1.90 Hz for the bottom row. These 12 frequencies were separated
by 0.12 Hz. At the center of each circle appeared a numeral from 0 through 9, the word
“SPACE,” and the symbols “<” or “” with a viewing-angle size of 0.5˚and a fixed lumi-
nance of 16.4 cd/m
2
. The participants started each trial by pressing the start button. First,
at the center of the gray screen appeared for 2 s a numeral or character, which instructed
the participant to gaze at the corresponding circle during the following trial. The 12 sti-
muli (Fig 1c) were then presented for 8 s each, during which time the participants gazed
at the predesignated circle. Prior to this experiment, each participant took part in a prac-
tice session.
Eye-gaze information input based on pupillary response
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4. Results and discussion.
1. Experiment 2a: Communication interface with two response options
The goal of experiment 2a was to identify at which circle the participants gazed based
on pupil-size oscillation measured with a visual display. Fig 5 shows typical PSD results
obtained with 0.01 Hz intervals. These results were constructed from the DFT of 7 s of
time-series data of pupil response for one participant gazing at the right circle. The results
show the PSD for differences in luminance-modulation frequencies between the two circles
of Δf= 0.06, 0.12, and 0.25 Hz. The blue and red lines indicate the PSD at the luminance-
modulation frequency of the left and right circles, respectively. These results show that, in
all of the trials, the PSD of the luminance-modulation frequency (red line) of the gaze-tar-
geted circle (i.e., the right circle) exceeded that of the left circle (blue line). This indicates
Fig 5. Experiment 2a: Example of DFT of time-domain pupil modulation results for oneparticipant and for each
frequency condition in which eye gaze was directed at the right circle.
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that, even when the difference between the luminance-modulation frequencies of the gaze-
targeted stimulus and adjacent (i.e., non-gaze-targeted) stimuli is relatively small (0.06,
0.12, 0.25 Hz), it is possible to identify the gaze-targeted stimulus based on the pupil
response.
Fig 6 shows the accuracy with which the gaze-targeted visual stimulus is identified
(called the “identification accuracy”) averaged over all participants for each frequency com-
bination. The gaze-targeted stimulus is identified by comparing the PSD of the luminance-
modulation frequencies of the two circles. Based on these results, we conclude that the
gaze-targeted object can be identified with at least 85% accuracy except just one condition
(Δf= 0.06Hz, luminance-modulation frequency = 2Hz) tested in this experiment. Fig 7
Fig 6. Average identification accuracy as a function of luminance-modulation frequency.
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Fig 7. Experiment 2a: Average identification accuracy as a function of left-right frequency difference Δf.
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shows the identification accuracy as a function of the frequency difference Δfbetween the
left and right circles for all base frequencies. The gaze-targeted stimulus was identified by
comparing the PSD of the luminance-modulation frequencies of the two circles. In other
words, we assume that, when a participant gazed at a circle with a certain luminance-modu-
lation frequency, the PSD for the given frequency increased.
For each frequency condition and for participants following the instructions regarding
gaze position, we calculated the accuracy of the identification of the gaze-targeted stimu-
lus based on the pupil response. The identification accuracy averaged over participants
was 89.4%, 98.8%, and 98.1% for the frequency difference Δfof 0.06, 0.12, and 0.25 Hz,
respectively. We used a single-factor analysis of variance to investigate the quantitative
effect of the frequency difference between gaze-targeted and non-gaze-targeted visual sti-
muli and found a significant effect [F (2,47) = 9.28, p <0.01]. The results of multiple com-
parisons based on Fisher’s protected least significant difference method reveal that the
differences in the results for Δf= 0.06 Hz and Δf= 0.12 Hz, and for Δf= 0.06 Hz and
Δf= 0.25 Hz are significant at the level of 1%. Based on these analyses, a reliable estimate
(98% accuracy) from the present method requires a minimum difference in luminance-
modulation frequency between the two circles of 0.12 Hz. In experiment 2a, we identified
the gaze-targeted circles (L circle or R circle) by comparing the frequency of the PSD peak
of the pupil-size oscillation with the luminance-modulation frequencies of two circles
without applying the correction (4). As shown in Fig 6, the identification accuracy is very
high. In fact, recalculating the prediction with the correction (4) included does not change
the results, which we attribute to the small difference Δfin the luminance-modulation fre-
quencies of the two circles. For greater differences Δfin the luminance-modulation fre-
quencies, the correction method should be included for a more reliable comparison
between the two PSDs.
2. Experiment 2b: Information-input interface with 12 options
Experiment 2b simultaneously compared 12 circles with different luminance-modulation
frequencies and examined the identification accuracy of the gaze-targeted circle. Fig 8
shows typical PSDs calculated with 0.01 Hz, DFT sampling intervals for time-domain data
spanning 7 s of pupil response. The results are given for each frequency condition for one
participant. The red lines indicate the luminance-modulation frequency of the gaze-tar-
geted circle. These results show that, in most of the cases, one of the PSD peaks corresponds
to the luminance-modulation frequency of the gaze-targeted stimulus. In other words, even
when simultaneously presenting 12 visual stimuli with different luminance-modulation fre-
quencies, the pupil size synchronizes to the luminance-modulation frequency of the gaze-
targeted stimulus.
However, more often than not, the PSD peak at the luminance-modulation frequency of
the gaze-targeted stimulus is a minor PSD peak. Therefore, we apply the data-correction
method developed in experiment 1 to increase the identification accuracy. Specifically, the
PSD functions shown in Fig 8 are multiplied by the weight ωgiven in Eq (4), and the fre-
quency with the highest corrected PSD is taken as the frequency for identifying the gaze-
targeted stimulus. Fig 9 shows the identification accuracy for each of the 12 luminance-
modulation frequencies averaged over all participants, and Table 3 lists the accuracy aver-
aged over all frequencies for each participant. These results indicate that information input
is possible for all of participants tested with at least at 60% accuracy. Note that, upon exclud-
ing the results for 0.58 Hz because the identification accuracy is quite low (62.5%) at this
frequency, the average accuracy reaches 87.5%.
Eye-gaze information input based on pupillary response
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Discussion
This study proposes an information-input interface that uses pupillometry and DFT analysis
and focuses on the synchronization of pupil-size oscillation with luminance modulation of visual
stimuli. We experiment with an interface with two response choices and an information-input
Fig 8. Experiment 2b: Typical PSD as a function of frequency for each frequency condition for a single
participant.
https://doi.org/10.1371/journal.pone.0226991.g008
Fig 9. Experiment 2b: Identification accuracy averaged over all participants for the 12 luminance-modulation frequencies.
https://doi.org/10.1371/journal.pone.0226991.g009
Eye-gaze information input based on pupillary response
PLOS ONE | https://doi.org/10.1371/journal.pone.0226991 January 9, 2020 13 / 18
interface with 12 response choices and evaluate the accuracy with which information can be
input using the proposed method. Although pupil size is well known to oscillate in response to
periodic luminance modulation of visual stimuli [see, e.g., [16] [17] [18] [19] [20]], no reports
exist that detail the correspondence between the pupil-oscillation frequency and luminance-
modulation frequency of stimuli in an information-input interface. In addition to the proposed
information-input interface, we report several important findings regarding the pupil response
to visual stimuli with various luminance-modulation frequencies.
In experiment 1, we examine the basic frequency characteristics of the pupil response by
exposing the participants to a single circular object with a luminance-modulation frequency
from 0.25 to 3.0 Hz. The analysis results are consistent with those from previous studies, which
reported, for participants aged 20 to 30 years, synchronization between the frequency of oscil-
lations in participant pupil size and the luminance-modulation frequency up to 3.15 Hz [see,
e.g., [22]]. The PSD obtained from the DFT of the time-domain data depends on the frequency
condition and, based on the results of a nonlinear regression analysis, can be approximated by
an exponential function with a high degree of explanatory power. This result is attributed to
the pupil-size modulation lessening with increasing luminance frequency. The PSD results
were thus corrected for this effect in order to compare the PSD for stimuli with different lumi-
nance-modulation frequencies and select the frequency that produces the greatest PSD. Upon
applying this correction method [see Eq (4)], the accuracy with which the gaze-targeted stimu-
lus is identified based on its luminance-modulation frequency is 90% or more for frequencies
from 0.75 to 2.75 Hz. Identification accuracy is 90% at 0.25 Hz and 80% at 0.5 Hz. At 3 Hz, the
identification accuracy drops to 30%. From these considerations, we conclude that luminance-
modulation frequencies from 0.75 to 2.25 Hz are optimal for a gaze-input system. The reason
why the identification accuracy was low in the less than 0.5 Hz, would be that the change of
pupil size is affected by the change in heart beat and respiration due to changes in the activa-
tion of the sympathetic nervous system that occur in the range of 0.15 to 0.40 Hz [25] [26]
[27]. From 0.75 to 2.75 Hz, the visual stimulus may be identified with the proposed methods
based on the gaze with an accuracy of 90%. Furthermore, we propose an algorithm to generate
input information based on the data obtained.
In experiment 2a, we examined the effectiveness of an interface with two response choices.
Participants gazed at one of the two visual stimuli in the display and the gaze-targeted stimulus
was identified by comparing the measured frequency of pupil-size modulation with the lumi-
nance-modulation frequency of the gaze-targeted stimulus. The results demonstrate an identi-
fication accuracy of 89.4% for the difference Δf= 0.06 Hz between the luminance-modulation
frequencies of the stimuli, which rises to 98% or more for Δf= 0.12 and 0.25 Hz. These results
demonstrate the effectiveness of the proposed method and indicate that the pupil diameter
becomes synchronized to the luminance modulation of the gaze-targeted stimulus rather
than to that of adjacent, non-gaze-targeted stimuli. It was recently shown that the PLR is
also affected by the luminance modulation of nearby, non-gaze-targeted stimuli [12] [28] [29].
Therefore, we consider that the proposed method is more efficient and reliable when partici-
pants direct both gaze and attention to a given visual stimulus.
Experiment 2b investigated the effectiveness of the proposed algorithm applied to an infor-
mation-input interface containing 12 items presented in a keyboard configuration. Based on
Table 3. Experiment2b: Identification accuracy for each participant averaged over all luminance-modulation frequencies.
Participant No. A B C D E F G H Average
Accuracy rate [%] 100 66.7 100 83.3 100 75 66.7 91.7 85.4
https://doi.org/10.1371/journal.pone.0226991.t003
Eye-gaze information input based on pupillary response
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the results of experiment 1, the luminance of the visual stimuli was modulated at frequencies
ranging from 0.58 to 1.9 Hz. The results show that the identification accuracy averaged over all
participants was 85.4%, which indicates that the pupil-size oscillation becomes synchronized
to the luminance-modulation frequency of the gaze-targeted stimulus (3˚viewing angle), even
if neighboring stimuli have differing luminance-modulation frequencies with a separation of
1˚. However, the identification accuracy for the lowest luminance-modulation frequency of
0.58 Hz is only 62.5%, so we conclude that an appropriate range of luminance-modulation fre-
quency for visual stimuli is from 0.7 to 1.9 Hz for a reliable and accurate information-input
interface. Some further issues remain to be discussed to improve the proposed method. The
first issue pertains to the individual differences observed in the accuracy with which the stimuli
are identified. Although three participants had identification accuracies of 100% in experiment
2b, two participants had identification accuracies around 67%. One possible cause for this
individual difference is a difference in experience with the interface. This issue is especially
important when developing a human interface for handicapped people. We must develop an
interface that all patients can use with ease without special experience or training. The second
issue to consider is the interface design, which includes the stimulus configuration and the
algorithm for choosing a gaze-targeted object. In experiment 2b, we arranged the 12 stimuli so
that the luminance-modulation frequency increased from left to right and from top to bottom.
However, this arrangement may not be optimal because the configuration of the stimuli and
the procedure design should make the algorithm more accurate and allow the development of
an easy-to-use interface. In addition, in this study, the luminance of the visual stimulus was
modulated by a sine wave to reduce participant stress. However, a square-wave modulation
may improve the accuracy because pupil size reportedly changes more under square-wave
modulation of the luminance of the stimulus [18]. Finally, the third issue is how attention
and gaze position affect the ability to direct the gaze at an object whose luminance is being
modulated. As mentioned above, recent reports claim that the PLR is affected by the lumi-
nance of a visual stimulus in a neighboring position, even if the eye is not directed at that posi-
tion [28] [29].
In the present study, the participants were instructed to direct both eye and attention to the
visual stimulus, which helped to accurately identify the gaze-targeted object without being dis-
tracted by the luminance modulation of adjacent stimuli. However, if distracting objects are in
the field of view, the accuracy with which gaze-targeted objects are identified might decrease.
Conversely, the use of attention only without directing gaze toward an object may suffice as
input. Such an interface would be helpful for locked-in patients. Therefore, further detailed
investigations are warranted to look into how eye gaze and attention can be exploited to
improve the information-input interface.
Changes in pupil size are known to depend on several factors. Psychological factors, such as
alertness level [6], emotions [30] [31] [32], and mental workload [33] [34], affect the mediation
of pupil size by the autonomic nervous system. Additionally, the mean steady-state pupil size
reportedly decreases with age [35]. The impacts of these factors must be investigated to employ
our proposed system in the future. This will require experiments involving many participants
with different demographic characteristics, such as gender, age, and living environment.
Compared with other techniques for information-input interfaces that use biological sig-
nals, such as EEG, MEG, or optical topography, pupillometry has some important benefits.
The proposed method for implementing an information-input interface using pupillometry
puts a low burden on users, has minimal invasiveness, requires no training or experience,
has high theoretical validity, and requires no calibration. However, online analysis will
be required for real-life application of this method. In fact, we have begun performing
online analysis. The results appear to be reliable [36], although we have not yet collected a
Eye-gaze information input based on pupillary response
PLOS ONE | https://doi.org/10.1371/journal.pone.0226991 January 9, 2020 15 / 18
sufficient amount of data. In the near future, we hope to develop a complete system that
functions online.
Conclusions
This study demonstrates an information-input interface that uses the synchronization of pupil
oscillation with the luminance modulation of visual stimuli to identify the stimuli. The method
identifies the gaze-targeted object from among many objects with differing luminance-modu-
lation frequencies. The use of pupillometry for uncalibrated eye tracking in HCI has several
possible practical applications. This method may be helpful for the design of interfaces that
allow patients with severely limited motor function to communicate clearly with others.
Acknowledgments
We thank Shoma Ichino, Junki Someya and Tsubasa Tanaka for their contribution in various
stages of this project.
Author Contributions
Conceptualization: Yumiko Muto, Hideka Miyoshi, Hirohiko Kaneko.
Data curation: Yumiko Muto, Hideka Miyoshi.
Formal analysis: Yumiko Muto.
Funding acquisition: Hirohiko Kaneko.
Investigation: Yumiko Muto, Hideka Miyoshi, Hirohiko Kaneko.
Methodology: Yumiko Muto, Hideka Miyoshi, Hirohiko Kaneko.
Writing – original draft: Yumiko Muto.
Writing – review & editing: Yumiko Muto, Hirohiko Kaneko.
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Eye-gaze information input based on pupillary response
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... Hybrid BCI can improve the classification accuracy, increase the number of commands, and shorten the detection time of the BCI system by combining two or more patterns (at least one of which is a brain signal) (Hong and Jawad, 2017). Recently, pupillary responses (PR), such as the pupillary light reflex, have been used as the second pattern in addition to EEG due to the low user burden, non-invasiveness, and no need for training (Muto et al., 2020). Pupil diameter changes steadily with the illuminance of the observed object to regulate the amount of light entering the eye (Crawford, 1936;Woodhouse, 1975;Woodhouse and Campbell, 1975), and the modulation frequency of PR is synchronized with the luminance-modulation frequency of the visual stimulus. ...
... Pupil diameter changes steadily with the illuminance of the observed object to regulate the amount of light entering the eye (Crawford, 1936;Woodhouse, 1975;Woodhouse and Campbell, 1975), and the modulation frequency of PR is synchronized with the luminance-modulation frequency of the visual stimulus. The amplitude of PR decreases as the stimulation frequency increases (Muto et al., 2020), and the consistent, measurable PR can be induced at the flickering frequency up to 2.3 Hz (Naber et al., 2013). Compared with the detection of gaze position Yao et al., 2018), the measurement of PR does not require system calibration. ...
... They also established a binary communication based on PR and achieved an accuracy of 100% at 10 bpm and 96% at 15 bpm. Muto et al. (2020) realized an information input interface with 12 options (from 0.58 to 1.90 Hz, with an interval of 0.12 Hz) based on PR. The averaged power spectral density (PSD) peak decreased with increasing luminance-modulation frequency, and the averaged classification accuracy reached 85.4% with a data length of 7 s. ...
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We have developed a new mono/binocular eye tracking system by using an IEEE1394b or USB-3.0 digital camera that provides high sensitivity, high resolution, high frame-rate and no rolling shutter distortion. Our goal is to provide a system that is friendly to researchers who conduct experiments. The system is non-invasive and inexpensive and can be used for mice, marmosets, monkeys, and humans. It has adopted infrared light to illuminate an eye (eyes). The reflected image of the infrared light on the cornea and the black image of the pupil are captured by the camera. The center of the pupil and the center of the corneal reflection are calculated and tracked over time. The movement of the head is compensated by the reflection. Since the high resolution camera has a 2048 horizontal pixels resolution, we can capture the images of both eyes simultaneously and calculate the parameters of the two eyes at each frame. The gaze position data can be read out on-line via computer network and/or DAC (digital analog converter). The adoption of the Windows 10 as the operation system makes this eye tracking system user-friendly. Because of the high frame-rate of the digital camera, the sampling rate of the system can be as high as 700 Hz and the latency less than 4 ms.
Chapter
The accepted classical view of the pupil response to light is that the ambient light level determines largely the steady-state size of the pupil (Lowenstein et al, 1964) and that rapid increments in light flux on the retina cause a brisk constriction of the pupil, that is often described as the dynamic pupil light reflex response (Stark & Shermann, 1957; Alexandridis, 1985; Lowenfeld, 1993). The afferent pathways involved in the control of the pupil in man have been associated with subcortical projections and this is consistent with clinical observations which suggest that the pupils continue to respond normally to sudden changes in room illumination even when the patients are corticaliy blind (Brindley et al, 1969). The response of the pupil often represents an important measurement in neurological and ophthalmologic examinations, but the poor understanding of the visual pathways involved and the kind of stimulus characteristics that cause pupillary responses limit the usefulness and potential use of such tests. Animal studies have contributed significantly to our understanding of the afferent neural pathways that subserve the Pupil Light Reflex response (PLR) in man and helped to reinforce the accepted classical view. Lesion studies combined with measurements of pupil responses before and after surgery in monkey have demonstrated the direct invol vement of the pretectal olivary nuclei and the Edinger-Westphal nuclei in both the steady state control of pupil size and the dynamic PLR response (Pierson & Carpenter, 1974). In rat, the control of the pupil response is somewhat less complicated and functionally more consistent with the regulation of retinal illuminance (Clarke & Ikeda, 1985a, b). The pupil diameter follows an almost linear relationship when plotted as a function of the logarithm of retinal illuminance over a wide range.