Motomura et al.
Journal of Physiological Anthropology(2023) 42:19
https://doi.org/10.1186/s40101-023-00335-2

ORIGINAL ARTICLE

Journal of
Physiological Anthropology

Open Access

Effects of others’ gaze and facial expression
on an observer’s microsaccades and theirassociation with ADHD tendencies
Yuki Motomura1*†, Sayuri Hayashi2,3†, Ryousei Kurose2, Hiroki Yoshida2, Takashi Okada3 and Shigekazu Higuchi1

Abstract
Background The aim of this study was to examine the effect of others’ gaze on an observer’s microsaccades. We
also aimed to conduct preliminary investigations on the relationship between the microsaccadic response to a gazeand a gazer’s facial expression and attention-deficit/hyperactivity disorder (ADHD) tendencies.
Methods Twenty healthy undergraduate and graduate students performed a peripheral target detection task
by using unpredictable gaze cues. During the task, the participants’ eye movements, along with changes in pupil
size and response times for target detection, were recorded. ADHD tendencies were determined using an ADHD
questionnaire.
Results We found that consciously perceiving the gaze of another person induced the observer’s attention; moreover, microsaccades were biased in the direction opposite to the gaze. Furthermore, these microsaccade biases weredifferentially modulated, based on the cognitive processing of the facial expressions of the gaze. Exploratory correlation analysis indicated that microsaccade biases toward gazes with fearful expressions may specifically be correlatedwith participant characteristics, including inattention.
Conclusions Our findings support that microsaccades reflect spatial attention processing and social cognitive processing. Moreover, the exploratory correlation analysis results suggested the potential benefit of using microsaccadebias toward spatial attention to assess pathophysiological responses associated with ADHD tendencies.
Keywords Microsaccades, Attention, Gaze, Emotion, Oculomotor control, Attention-deficit/hyperactivity disorder†

Yuki Motomura and Sayuri Hayashi contributed equally to this work.

*Correspondence:
Yuki Motomura
motomura@design.kyushu-u.ac.jp
1
Department of Human Life Design, Faculty of Design, Kyushu University,
4‑9‑1 Shiobaru, Minamiku, Fukuoka 815‑8540, Japan2
Department of Kansei Science, Graduate School of Integrated Frontier
Science, Kyushu University, 4‑9‑1 Shiobaru, Minamiku, Fukuoka 815‑8540,
Japan
3
Department of Developmental Disorders, National Instituteof Mental Health, National Center of Neurology and Psychiatry, 4‑1‑1,
Ogawahigashi, Kodaira, Tokyo 187‑0031, Japan

Background
Very small unconscious eye movements occur whenhumans gaze at an object. These miniature movements
have been reported as randomly occurring oculomotor
phenomena and are considered fixational eye movements. Fixational eye movements are subdivided, basedon their dynamic characteristics, as follows: tremors
with small and high frequencies, drifts with large andslow movements, and microsaccades with saltatory
characteristics similar to normal eye movements (i.e.,saccades) [1, 2]. These movements are involved in counteracting retinal adaptation by randomly displacing the© The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which
permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to theoriginal author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images orother third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line
to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory
regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of thislicence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/. The Creative Commons Public Domain Dedication waiver (http://​creat​iveco​
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retinal image and refreshing the stimulus input into theretinal nerves [3].
Spatial attention and saccade movements are closely
related and have partly common neural mechanisms[4–6]. Engbert et al. [7] investigated the effect of spatial attention shifts on microsaccades. They found thatmicrosaccades orient toward spatial attention induced byspatial cues in a subsequent phase with increasing microsaccades (i.e., rebound phase), after the initial inhibitionof microsaccades [7]. Their findings suggest that microsaccades, which are lower-order oculomotor phenomena
for visual maintenance, may be associated with higherorder cognitive functions. Subsequent studies have demonstrated that microsaccades reflect various higher-ordercognitive processes, including attention. For example,
Valsecchi et al. [8] examined microsaccade activities
using an oddball task and reported differences in temporal patterns in microsaccadic frequencies between oddball and standard stimuli. In particular, they reported
prolonged initial inhibition of microsaccades in response
to oddball stimuli requiring recognition and memory(i.e., counting the number of oddballs) [8]. Additionally, Kashihara et al. [9] reported that unpleasant stimuli
inhibited microsaccade occurrence in the rebound phase;moreover, they suggested that the microsaccades are oriented to the opposite side of unpleasant stimuli during
the rebound phase.
The microsaccade direction in the rebound phase isinfluenced by the spatial attention direction. Of note,microsaccade bias is dependent on the type of attention[7, 10–12], especially on the mode (i.e., endogenous orexogenous) [13]. If an arrow indicating the target positionon either side is shown and spatial attention is intentionally moved to the arrow-indicated direction, the modeis endogenous attention. However, if a flash suddenly
appears around the visual field and reflexive attention
is given, the mode is exogenous attention. Endogenous
attention is a top-down process, based on the internal
state and conscious expectations. By contrast, exogenous attention is a bottom-up process reflexively controlled by prominent external sensory events [14]. The
microsaccade direction is biased toward the direction ofendogenous attention. The microsaccade direction after
presenting stimuli that provide spatial cues is biased
toward the endogenous attention shift [7]. The sudden
appearance of peripheral stimuli that attract exogenous
attention conversely causes microsaccade biases in the
direction opposite to that of the attention shift [15, 16].
Two main interpretations exist regarding the mechanisms underlying microsaccade bias in the direction
opposite to that of exogenous attention. One interpretation is that microsaccade bias reflects an attention shift due to “inhibition of return” (“IOR”) [17, 18],a phenomenon in which attention is inhibited from“returning” to the position where the attention waspreviously directed [19]. This facilitates attention to beprovided to a position in the visual field without previous attention [19]. For example, in a task where thepreceding peripheral stimuli and subsequent target
stimuli are spatially matched, IOR is presumed to haveoccurred when a delayed reaction occurs in the previous attention direction. Another interpretation is the“inhibition hypothesis” where in case maintaining fixation is necessary, inhibiting automatic saccades induced
by exogenous stimuli causes microsaccade directional
bias [20]. This hypothesis is based on the finding that
inhibiting reflex saccades causes bias in oculomotor
neuron activation to movements into the contralateralvisual field [21] in processing for integrating information of the saccade direction in the superior colliculus[22]. However, these hypotheses regarding the opposite
microsaccade bias due to exogenous attention remain
unclear.
When observing another person’s gaze, attention is
guided in the direction of that gaze. This automatic
attention orientation involves subcortical oculomotor
systems, including the superior colliculus, which controls eye movements such as saccades [23]. Studies have
demmonstrated that others’ eyes affect an observer’s
attention and eye movements [23–25]. In a saccade taskusing gaze cues, the required reaction times and saccade
accuracy are enhanced when the others’ gaze direction
matches the target position [25, 26]. By contrast, inconsistent gaze directions have an interference effect ontask performance [27]. Whether this automatic attention
orientation induced by eye gaze reflects endogenous orexogenous attention remains under discussion. Previous
studies have demonstrated that nonsocial spatial cues(e.g., arrows) trigger endogenous spatial attention [9, 28].
Findings of another review study [29] indicate that socialspatial cues (e.g., eye gaze) also automatically guide spatial attention; however, this attentional processing may
differ from endogenous attention. Moreover, a recent
study [30] showed that attention orientation inducedby eye gaze resembled exogenous attention rather thanendogenous attention, which suggested an association of
attentional processing triggered by eye gaze with exogenous attention.
The automatic saccade control mechanism based onanother person’s gaze is considered crucial for quickly
detecting others’ interests and potential dangers. Saccades started and stopped by social cues (other person’sgaze) are more resistant to inhibition by interference
stimuli, compared to those started and stopped by nonsocial cues (e.g., color changes) [31]. This finding suggests
the biological importance of the other person’s gaze.

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Thus, neural networks associated with such attention
and saccade control may have neural structures specialized in processing social signals, especially information
obtained from others’ gaze [32]. Furthermore, microsaccades controlled by the superior colliculus, including saccades, can be modulated by spatial attention generated
by perceiving others’ gaze direction and may reflect thesocial value of gaze information. Exogenous attention
caused by emotional stimuli and prominent visual stimuli
that suddenly appear in the peripheral vision modulate
the microsaccade direction and microsaccadic rates [9,15, 16]. However, it remains unclear whether stimuli withleft or right gaze and emotional facial expressions modulate these microsaccade activities. Others’ gaze contains
crucial information for survival and is thought to bemodulated by others’ emotions. For example, anotherperson’s fearful gaze may act as a signal of a potential
threat ahead, and the ability to perceive this gaze may
have adaptive significance. One of our study objectives
was to investigate how microsaccades, which are involuntary eye movements related to attentional functions,are affected by neutral or fearful gaze. Moreover, microsaccades, which are associated with both attentional andemotional processing, may be beneficial for the assessment of pathophysiological responses associated withproblems in social and attentional function [9].
Attention-deficit/hyperactivity disorder (ADHD) is
one of the most common neurodevelopmental disorders.
ADHD is characterized by inattention and/or hyperactivity-impulsivity persistent from childhood [33]. The estimated prevalence of ADHD in adults is approximately
2.5% [34]. Compared to typically developed adults, somestudies have suggested that adults with ADHD have ahigher risk of facing social problems such as divorce [35],substance abuse [36, 37], driving accidents [38, 39], sexual problems [34, 40], and job changes [35]. These risks
in adults with ADHD may be associated with a complex
interplay of multiple factors, including cognitive deficits(i.e., impaired executive function [41] and reward systems [42]), developmental history, and social and medical
support.
In addition, some studies have reported deficits insocial cognitive processing in ADHD [43–45] withabnormality in oculomotor control [46]. One study [47]also reported that adults with high ADHD tendencies
made more errors in a saccade task requiring oculomotor
inhibitory control (i.e., antisaccade) and cognitive processing of social cues (i.e., others’ facial expressions) than
did adults in the control group. Another study [48] demonstrated that attention loads are inversely correlatedwith the microsaccadic rate, which supports that the
microsaccadic rate (i.e., the number of microsaccades per
second) reflects the cognitive/attention processing level[12, 48]. Moreover, ADHD studies have reported a lower
microsaccade inhibition rate in patients with ADHD thanin individuals with typical development, which suggeststhat microsaccades reflect deficits in attentional function
in patients with ADHD [49, 50]. Thus, oculomotor control, including microsaccades strongly associated withsaccades [51], possibly characterizes social and attentional function, which may be useful for developing biological assessment for social and attentional dysfunction
in individuals with high ADHD tendencies.
As previously mentioned, numerous studies haveinvestigated microsaccades for spatial attention; however, few studies have investigated the effects of perception/attention on microsaccades resulting from social
factors. Additionally, microsaccades may reflect an individual’s attentional function and different modulations
may be prominent, especially in spatial tasks requiring
cognitive processing of social cues. Therefore, this study
aimed to examine whether differences in facial expressions affect the microsaccadic rates, and whether others’
gaze modulates microsaccade direction. Additionally,
we aimed to examine whether microsaccade biases differ, depending on the gazers’ facial expressions. Basedon previous findings indicating that negative emotional
pictures suppressed the microsaccadic rate during therebound period [9, 28], we expected that a face withnegative expression would induce a lower microsaccadic
rate than would a neutral face. Additionally, based on a
recent study [30] demonstrating that attention orientation induced by social cues resembled that induced byreflexive exogenous cues, we expected that the microsaccade direction would be biased for opposite to gaze
directions. We also expected that this directional bias
would be enhanced by fearful expression (implying fear
located toward the gaze) because the direction of the
microsaccadic response is biased opposite to fear [9, 28].
For preliminary and exploratory examinations of the utility of microsaccades as a biomarker of ADHD tendencies, we aimed to investigate the relationship between the
microsaccadic response to the gaze and the gazer’s facial
expression and personal characteristics, determined byusing an ADHD questionnaire.

Methods
Participants

We enrolled 20 healthy male university students [meanage (standard deviation [SD]): 22.90 (0.91) years old]from Kyushu University (Fukuoka, Japan). We recruitedmale students on account that sex possibly affects attentional processing for eye gazes [52] and emotional signals[53], and difficulties in conducting experiments using
female individuals (e.g., obtaining information about
menstrual cycles or changing participants’ clothes for theMotomura et al. Journal of Physiological Anthropology(2023) 42:19

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experiments). After receiving explanations regarding theexperiment’s purpose, the participants provided writtenconsent. This study was approved by the Research Ethics
Committee of Kyushu University.

point subsequently reappeared in the center for 800 ms;
the target stimuli (“T”, size: 0.7° × 0.7°) were presented at
the left or the right box. The participants were instructedto promptly report the target stimulus location (i.e., leftor right) by pressing the left and right control keys on the
keyboard with their index fingers. The target stimulus
was displayed until the response. The task interval was
set at 4 s.
The experiment comprised six blocks. Each block consists of 48 trials. Within each block, each facial stimulus(a total of 24 stimuli: two facial expressions × two gaze
directions × six models) was presented two times. The
position of the target stimuli was presented, regardlessof the gaze direction of the previously presented face
image (50% matches the gaze direction). Additionally, theprogram was controlled to ensure the same number ofmatching and mismatching trials in each block. Moreover, the participants were informed that the gaze point ofa presented face would be irrelevant to the target direction. Further, they were instructed to always adjust the
viewpoint to the gaze and to avoid extensively blinking
during the stimulus presentation.

Stimulus presentation

To present the stimuli, we selected images of six models(three male models and three female models) with neutral and fearful facial expressions from the standard facial
expression stimuli set [54]. To control gaze direction, theirises and pupils of the original facial image were moved
to the right or left using Adobe Photoshop CC 2018. The
background and model hair were removed after cropping
the images into oval shapes with a width of 3.3° and aheight of 4.4°. Stimulus presentation and behavioral dataacquisition (i.e., response times) were controlled using
software (Presentation; Neurobehavioral Systems, Berkeley, CA, USA) on a personal computer.
Procedure

After providing informed consent, the participantschange their clothes for the experiments. Then, the participants completed a questionnaire regarding their personality traits and drowsiness. They subsequently sat infront of a display with the height of the chin rest adjusted
to achieve a comfortable position. After calibrating themeasuring instrument, a peripheral target detection task
was conducted using the procedure shown in Fig. 1 (a).
The stimulus presentation was started with a white gazing point (・, viewing angle: 0.19°) and two boxes (□, size:
2° × 2°; line width: 0.35°; distance from the gaze point:8°) on a gray background presented for 1000–1500 ms,
as shown in Fig. 1 (a). The face images (neutral or fearful expression, left or right gaze) randomly selected fromthe dataset were then presented in the display centerfor 200 ms. After the facial image disappeared, the gaze

Fig. 1 Example of a stimulus presentation sequence and experiment scene

Experiment environment

The experiment was conducted in a soundproof/electromagnetic-shielded artificial climate room (set temperature: 25 °C; relative humidity: 60%) in the Environmental
Adaptation Laboratory, Ohashi Campus, Kyushu University [Fig. 1 (b)]. The laboratory was equipped with a web
camera for observation, a 24-inch liquid crystal display(BENQ XL2411P; BenQ Corp.; Taipei, Taiwan) for presenting images, an electroencephalographer, a keyboard
for responses, and an eye-movement-measuring instrument (Tobii Pro Spectrum; Tobii Technology KK, Stockholm, Sweden). The presentation display was positioned
so that the distance between the participants and theMotomura et al. Journal of Physiological Anthropology(2023) 42:19

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gaze point was 75 cm. Additionally, the keyboard position was adjusted for each participant to allow them topress keys while seated with a comfortable posture.

analyzed pupil diameters to evaluate the alertness levelby stimuli of the presented emotional facial expressions.
The time-series data of the pupil diameters were epochedin the interval from -200 ms to 1000 ms relative to theonset of facial stimulus presentation. Furthermore, forbaseline correction, the value of each sampling point was
divided by the mean value obtained within the -200 ms to
0 ms interval of each epoch.
With regard to the analysis of eye movements, we analyzed the interval from -200 ms to 1000 ms relative to theonset of a facial stimulus presentation from the tracking
data. By using a fixation filter attached to the tracking
analysis software [58], intervals where blinking or saccades occurred, as well as 100 ms before and after theinterval, were set as missing values. Moreover, we calculated the average eye angular velocity of 10 ms (i.e., a
20-ms time window) before and after each sample point.
An interval of ≥ 30°/s was labeled as the interval whensaccades occurred [58]. We excluded trials in which thedefective intervals exceeded 25% of the total in each task.
For the cleaned data, microsaccades were detected usinga binocular microsaccade detection algorithm [7]. Microsaccades are defined as ballistic binocular movements[59]. These feature values are within the range reportedby Martinez et al. [60]; therefore, the detected microsaccades were considered valid (see Supplementary file).
We excluded two participants: one participant had
technical problems in the eye movement measurement
and extremely few trials for analysis, whereas the otherparticipant had undetectable microsaccades. Finally, we
included 18 individuals [mean (standard deviation [SD])age: 22.83 (0.92) years old] in the analysis.
The microsaccade direction, peak velocity, and amplitude in each task were calculated. Furthermore, we compared the microsaccade rates and direction bias undereach facial expression condition.
Microsaccade rates were calculated as the microsaccade occurrence frequency with a 200 ms time window(i.e., 100 ms before and after) with a sampling interval of
1.7 ms (1/600 s). Polar plots were created to detect the
microsaccade directional bias. In addition to the reboundphase (i.e., 400–600 ms relative to the onset of facial stimulus presentation) [9], we analyzed the phase following
the rebound phase (800–1000 ms relative to the onset of
facial stimulus presentation) because attentional processing induced by emotional signals could persist after therebound phase [61]. The polar plots were calculated from
12 evenly spaced directional pins (every 30°) in which theangle of the horizontal axis across the center of the screen
was 0° (i.e., 180°). We set areas of interest (AOIs) as 120°
to 240° and -60° to 60°. An AOI on the same side of thegaze directions of a facial stimulus was set as “same.” Theother AOI on the opposite side of the gaze directions was

Measurement
Measurement of eye movements

Eye movements with a change in pupil size were tracked
using the eye-movement-measuring instrument (Tobii
Pro Spectrum, Tobii Technology KK; sampling rate,
600 Hz; accuracy, 0.3°; precision, 0.06°) and software(Tobii Pro Lab Version 1.98; Tobii Technology KK). A
standard five-point calibration was conducted at the startof the experiment.
Conner’s adult ADHD rating scale–Japanese version

The ADHD characteristics of the individuals were examined using the Japanese version of Conners’ Adult ADHD
Rating Scale (CAARS) [55]. The Japanese version of
CAARS evaluates 66 question items related to respondents’ behaviors and problems on a four-point scale. This
questionnaire yields an inconsistency index that evaluates the validity of answers to the eight subscales for
ADHD, including four factor-derived subscales, three
Diagnostic and Statistical Manual of Mental Disorders,Fourth Edition (DSM-IV) ADHD symptom subscales,
and an ADHD index. The four factor-derived subscales
are used to assess symptoms and behavior (i.e., inattention/memory problems, hyperactivity/restlessness,
impulsivity/emotional lability, and problems with selfconcept) across multiple domains. Moreover, the ADHD
symptom subscales of the DSM-IV is used to evaluate
ADHD symptoms (i.e., inattentive, hyperactive/impulsive, and total ADHD symptoms) based on the DSM-IV
criteria [56]. These ADHD indicators allow differentiating between individuals with and without ADHD.
The raw scores of these subscales were converted tostandard T scores on the corresponding profile paper andincluded for the analysis. The T scores are common to all
subscales and are used as the standard scores when themean value and SD of a large standard base (N = 2000)
are 50 and 10, respectively. The CAARS guidelines provide percentile values corresponding to T scores fordetermining the status of the examined person.
In this study, an inconsistency index score of ≥ 8 points
indicated an unnatural contradiction in the answer,
which was then excluded from the analysis, based on theguidelines.
Analysis method

Emotional stimuli changed the observer’s pupil diameter, based on their alertness level, which is attributed
to emotional alertness adjusting pupil diameter throughsympathetic nervous system activity [57]. Therefore, weMotomura et al. Journal of Physiological Anthropology(2023) 42:19

set as “opposite.” The microsaccade occurrence rate was
the number of microsaccades in each AOI (i.e., same or
opposite) divided by the total number of microsaccades.
We used this microsaccade occurrence rate as an index
of the microsaccade direction. Additionally, we calculated the microsaccade bias scores. The microsaccadebias score was the difference between the microsaccade
occurrence rates in two AOIs (i.e., same minus opposite).
Positive and negative values for the microsaccade bias
scores indicated bias in the same and opposite directions
as the gaze, respectively. To explore ADHD factors associated with these microsaccadic responses, we analyzed
the correlation of the microsaccade rates and bias in eachfacial expression with T scores for the eight ADHD subscales in the Japanese version of CAARS.
Statistics

We calculated the average values for participants in alltrials of each condition. We subsequently calculated thetotal average for all participants. All data are expressed as
the mean (SD). Statistical significance was set at p < 0.05;
moreover, p < 0.1 was taken as marginally significant. Statistical analyses were performed using R, version 3.5.2,
statistical software (R Foundation for Statistical Computing, Vienna, Austria) [62].
In the test for reaction time, we used repeated-measures two-way analysis of variance (ANOVA) (i.e., gazetarget congruence [congruent, incongruent] × facial
expression [neutral, fear]). In the test for pupil diameter changes and microsaccadic rates, we calculated theaverage pupil diameter and microsaccadic rate for eachinterval. We subsequently conducted a paired t-test to
analyze differences between the mean values of the facial
expressions.
Regarding the microsaccade directional bias, we conducted repeated-measures two-way ANOVA (i.e., microsaccade direction [same, opposite] × facial expression[neutral, fear]) for the microsaccade rate in each interval.
When an interaction existed, a simple main effect analysis with Bonferroni’s correction was conducted.
As the exploratory correlation analysis for the preliminary investigation on the relationships between microsaccadic responses and each scale of the Japanese versionof the CAARS, we calculated Pearson’s product-moment
correlation coefficient with testing of the significance ofthe correlation coefficient without multiple comparison
corrections.

Results
Reaction time

Table 1 shows the mean reaction time (RT) for eachexperimental condition. A two-way ANOVA with thegaze-target congruence and facial expression as factors

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Table 1 Average reaction time under each condition
NeutralCongruence

Fear

Congruent Incongruent Congruent Incongruent

Mean RT (ms) 306.60

310.80302.62

310.73

SD

37.02

32.99

33.00

32.78

RT reaction time, SD standard deviation

revealed a significant main effect of gaze-target congruence [F(1,17) = 8.58, p = 0.01, partial η2 = 0.34]. However,
the main effects of facial expressions [F(1,17) = 2.61,
p = 0.12, partial η2 = 0.] and interactions [F(1,17) = 1.59,
p = 0.22, partial η2 = 0.09] were not significant.
Pupil diameter

Figure 2 shows the time-series changes in the pupil diameter. For each facial expression, the pupil diameter began
decreasing at approximately 300 ms relative to the onset
of facial stimulus presentation, reached a minimum atapproximately 600 ms, and then returned to baseline.
To confirm the effect of facial expressions on pupil
diameter in the interval showing inhibition (i.e., 300–
1000 ms relative to the onset of facial stimulus presentation), we conducted a paired t-test by using themean value of the pupil diameter of each facial expression within this interval. However, we observed noeffect resulting from differences in facial expressions[t(17) = 0.51, p = 0.62, Hedges’ g = 0.03].
Microsaccade rates

Figure 3 (a) shows the time-series change in the microsaccade rates. The microsaccadic rates relative to theonset of a facial stimulus presentation (i.e., 0–200 ms)
decreased under each condition (i.e., neutral and fear)and subsequently increased beyond the baseline (i.e.,
400–600 ms, the rebound phase).
To verify the effect of facial expressions on the microsaccadic rates in each interval (i.e., -200 to 0 ms, 400 to
600 ms, and 800 to 1000 ms), we conducted a paired
t-test on the mean microsaccadic rates for each facial
expression. However, no effect of facial expression differences existed among the intervals from -200 ms to 0 ms[t(17) = -0.13, p = 0.90, Hedges’ g = -0.01], 400–600 ms[t(17) = 1.19, p = 0.25, Hedges’ g = 0.14], and 800–1000 ms[t(17) = -0.63, p = 0.54, Hedges’ g = -0.11].
Microsaccade directional bias (Microsaccade occurrence
rates in the same and opposite directions of gaze)

Figure 3 (b) presents the polar plots showing the microsaccade directions in which each facial expression
occurred within the target intervals (-200 to 0 ms, 400–
600 ms, and 800–1000 ms). In the interval from -200 ms

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Fig. 2 Time-series change in pupil size for each facial expression

Fig. 3 Time-series change in the microsaccadic rates and polar plots in microsaccade directions in each phase for each facial expression. Boxes
indicated by the dotted line in (a) show three intervals for further analysis

to 0 ms relative to the onset of facial stimulus presentation, which was the baseline, no main effect existed for
microsaccade direction [F(1,17) = 2.56, p = 0.13, partialη2 = 0.13] or facial expression [F(1,17) = 0.54, p = 0.47,
partial η2 = 0.03], and no interaction effect existed[F(1,17) = 0.01, p = 0.92, partial η2 < 0.001].
By contrast, in the interval from 400 to 600 ms relative to the onset of a facial stimulus presentation, themicrosaccade direction had a main effect [F(1,17) = 7.49,
p = 0.01, partial η2 = 0.31; Fig. 4]. However, no significant
main effect existed for facial expressions [F(1,17) = 0.42,
p = 0.52, partial η2 = 0.02] and interaction effect[F(1,17) = 0.23, p = 0.64, partial η2 = 0.01]. This finding
indicated that the observer’s microsaccades were biased
in the direction opposite to the gaze, regardless of differences in facial expressions.
In the interval from 800 to 1000 ms relative to the onset
of facial stimulus presentation, no significant main effects
existed for the microsaccade direction [F(1,17) = 1.07,
p = 0.32, partial η2 = 0.06] and facial expression[F(1,17) = 0.0008, p = 0.98, partial η2 = 0.001]. However, asignificant interaction effect existed between the microsaccade direction and facial expression [F(1,17) = 4.54, p = 0.05,
partial η2 = 0.21]. Simple main effect analysis revealed aMotomura et al. Journal of Physiological Anthropology(2023) 42:19

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presentation) and microsaccade directional bias (400–600 ms and 800–1000 ms, relative to the onset of facial
stimulus presentation) with the T scores of the eight subscales of the Japanese version of CAARS (i.e., inattention/
memory problems, hyperactivity/restlessness, impulsivity/emotional lability, problems with self-concept, DSMIV inattention problems, DSM-IV hyperactive/impulsive
symptoms, DSM-IV total ADHD symptoms, ADHD
Index). As shown in Table 3, correlations existed in the
microsaccade rate and microsaccade directional bias scorein the interval of 800 ms to 1000 ms relative to the onset
of presenting fearful expressions with inattention/memory problems (rate: r = -0.51, p = 0.03; bias score: r = 0.51;
p = 0.03), which indicated relationships between low microsaccadic responses (low rate and attenuated bias opposite
to the gaze) in the interval and high-score of the inattention/memory problems. Moderate positive correlations of
the microsaccade directional bias also existed in the interval from 800 to 1000 ms relative to the onset of presenting
fearful expressions with the problems with self-concept(r = 0.43, p = 0.07), DSM-IV inattentive symptoms (r = 0.58,
p < 0.001), and DSM-IV total ADHD symptoms (r = 0.44,
p = 0.07) (Fig. 6). In the interval from 400 to 600 ms, microsaccade directional bias was moderately positive in correlation with the problems with self-concept.

Fig. 4 Microsaccade direction between 400 and 600 ms relative
to the onset of facial stimulus presentation under each condition

higher proportion of microsaccades in the same direction
as the gaze induced by fear than neutral [F(1,17) = 7.76,
p = 0.01, partial η2 = 0.31; Fig. 5 (a)]. A simple main effectanalysis revealed that the effects of a direction is significant only in the neutral condition [neutral: F(1,17) = 4.59,
p = 0.05, partial η2 = 0.21; fear: F(1,17) = 0.44, p = 0.15, partial η2 = 0.12]. The mean (SD) microsaccade bias scores in
the neutral and fear conditions were -10.9 (21.6) and 3.24
(20.6), respectively. These findings showed that the microsaccade direction in the interval of 800 ms to 1000 ms wasbiased opposite to the gaze in the neutral condition.
Correlation with questionnaire CAARS

Table 2 shows descriptive statistics of the CAARS T scores.
Table 3 shows the results of the correlation analysis of the
microsaccadic rates for each facial expression (400–600 ms
and 800–1000 ms, relative to the onset of facial stimulus

Discussion
This study utilized a peripheral target detection task toevaluate spatial attention extrinsically caused by gaze andfacial expressions. Others’ gaze is known to automaticallyguide the observer’s attention, even if the subsequent target position is nonpredictive [63–66]. In this study, during the detection task, the effect of congruence between
the gaze and target direction was shown in the RT. In
particular, the RT was faster when the gaze direction andtarget position did not match than when they did match.
This findings indicates that the gaze of the facial stimuli
used in this study automatically guided the participants’spatial attention.
Previous studies [67–72] have reported that fearful facial expressions enhance attention in the eye gaze
direction; however, we did not observe a significant
effect of facial expression or facial-gaze interaction. Thisfindings could be attributed to the difference in stimulus-onset asynchrony (SOA) between facial and target
stimuli. In previous studies [68–72], most SOAs of thereaction tasks were < 500 ms; By contrast, the SOA in
our study was 1000 ms, which was approximately twice
as long because of the protocol setting for the microsaccade measurement. The onset of joint attention has previously been reported to begin within 200 ms relative tothe onset of the stimulus presentation; thus, the SOA waslonger in our study.

Motomura et al. Journal of Physiological Anthropology(2023) 42:19

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Fig. 5 Microsaccade direction between 800 and 1000 ms relative to the onset of facial stimulus presentation under each condition

Table 2 Summary of the CAARS T-scoreCAARS subscale (T-score)
A

B

C

D

E

F

G

H

Mean
(SD)

53.1 (9.4)

53.0 (8.5)

46.9 (6.8)

48.4 (6.7)

52.5 (6.7)

52.6 (9.6)

52.8 (9.6)

51.3 (9.0)

Min–Max

33–70

42–77

40–63

35–58

35–70

41–75

38–72

34–73

The letters A to H indicate the subscale of the CAARS, as follows: A, inattention/memory problems; B, hyperactivity/restlessness; C, impulsivity/emotional lability; D,
problems with self-concept; E, DSM-IV inattentive symptoms; F, DSM-IV hyperactive-impulsive symptoms; G, DSM-IV ADHD symptoms total; and H, ADHD index
CAARS Conners’ Adult ADHD Rating Scale, SD standard deviation, Min minimum, Max minimum

Time-series changes in the microsaccadic rates tofacial expressions [Fig. 3 (a)], comprised early inhibition (0–200 ms), followed by the rebound phase(400–600 ms). This microsaccade rebound is primarily
suppressed during tasks involving covert attention [7, 10,17]. Previous studies [8, 12] have reported microsaccade
rebound inhibition in visual and auditory oddball tasks.
By contrast, attention tasks using simple visual stimuli
such as arrows, light, and color, induce nonsignificant
or low rebound inhibition [7, 15]. Regarding microsaccades during the rebound period, Kashihara et al. [9]reported that emotional stimuli with dilated pupil diameter, especially those related to negative emotions, had astrong inhibitory effect. Given that emotional attention
can activate early brain processing, which is the subcortical pathway [73], Kashihara et al. [9] proposed that the
suppressed microsaccade rebound process for emotional
stimuli was caused by retaining previously important
information (e.g., threat information) at the expense of
the general update process with new visual inputs.
Contrary to our expectation that a fearful face would
attenuate the microsaccade rates in the rebound phase,

Motomura et al. Journal of Physiological Anthropology(2023) 42:19

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Table 3 Summary of correlation between microsaccade responses and CAARS
A

B

C

D

E

F

G

H

Microsaccade Neutral r = 0.30,
rate
p = 0.22(400–600 ms)

r = 0.35,
p = 0.15

r = 0.10,
p = 0.69

r = 0.11,
p = 0.67

r = 0.20,
p = 0.42

r = 0.25,
p = 0.31

r = 0.27,
p = 0.27

r = 0.27, p = 0.27

Fear

r = 0.13,
p = 0.61

r = 0.09,
p = 0.72

r = -0.14,
p = 0.58

r = 0.02,
p = 0.94

r = 0.08,
p = 0.75

r = 0.07,
p = 0.77

r = 0.18, p = 0.47

Neutral r = 0.38,
p = 0.12

r = 0.33,
p = 0.18

r = 0.36,
p = 0.14

r = 0.13,
p = 0.06
r = 0.04,
p = 0.87

r = 0.34,
p = 0.17

r = 0.20,
p = 0.43

r = 0.29,
p = 0.23

r = 0.32, p = 0.20

Fear

r = 0.06,
p = 0.82

r = 0.21,
p = 0.41

r = 0.24,
p = 0.33

r = 0.05,
p = 0.84

r = 0.02,
p = 0.94

r = 0.10,
p = 0.69

r = 0.07,
p = 0.78

r = 0.03, p = 0.91

Microsaccade Neutral r = -0.18,
rate (800–p = 0.47
1000 ms)r = 0.08,
p = 0.75

r = -0.19,
p = 0.44

r = -0.18,
p = 0.47

r = -0.24,
p = 0.33

r = 0.04,
p = 0.88

r = -0.10,
p = 0.70

r = -0.004,
p = 0.99

r = -0.51,
p = 0.03

r = -0.26,
p = 0.92

r = -0.24,
p = 0.33

r = -0.30,
p = 0.23

r = -0.34,
p = 0.16

r = -0.08,
p = 0.74

r = -0.23,
p = 0.35

r = -0.22,
p = 0.38

Microsaccade Neutral r = 0.08,
bias (800–p = 0.75
1000 ms)r = 0.16,
p = 0.52

r < 0.001,
p = 0.99

r = -0.17,
p = 0.51

r = -0.11,
p = 0.65

r = 0.06,
p = 0.81

r = -0.02,
p = 0.93

r = -0.2, p = 0.42

r = 0.51,
p = 0.03

r = 0.15,
p = 0.55

r = 0.17,
p = 0.50

r = 0.43,
p = 0.07

r = 0.58,
p = 0.01

r = 0.19,
p = 0.44

r = 0.44,
p = 0.07

r = 0.27, p = 0.28

Microsaccade bias
(400–600 ms)

Fear

Fear

The values of p < 0.05 and p < 0.10 are shown in red-bold and black bold, respectively. Letters A to H indicate the subscale of the CAARS, as follows: A, inattention/
memory problems; B, hyperactivity/restlessness; C, impulsivity/emotional lability; D, problems with self-concept; E, DSM-IV inattentive symptoms; F, DSM-IV
hyperactive-impulsive symptoms; G, DSM-IV ADHD symptoms total; and H, ADHD index
CAARS Conners’ Adult ADHD Rating Scale

Fig. 6 Correlations with microsaccade biases induced by fearful expressions from 800 to 1000 ms relative to facial stimulus onset

Motomura et al. Journal of Physiological Anthropology(2023) 42:19

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compared to a neutral face, we did not observe a significant difference in the microsaccadic rates during therebound phase when perceiving neutral and fearful facial
expressions (Fig. 4). This finding could be attributed tothe alertness of the evoked emotions. Kashihara et al. [9]used images from the International Affective Picture System [74] that could be perceived as direct threats such as
snakes and guns as unpleasant stimuli. Thus, the expansion rate of the pupil diameter, which is dependent on theemotional alertness degree [57], was significantly larger
in the unpleasant condition than in the neutral and pleasant conditions. By contrast, we observed no significant
difference in the change in pupil diameter between theneutral and fearful expressions (Fig. 2). The arousal levelof the induced emotions in our study could have been
lower than that of emotional images used by Kashihara
et al. [9]. If the microsaccade rebound process reflects theselective function of the importance of input visual information, then the visual information of emotional stimuli
in our study may have been difficult to selectively retain
because of low emotional alertness. However, whether
the criteria for information selection in the microsaccade
rebound process is based on emotional alertness or the
degree of emotional value remains unclear. Therefore,
further research is needed.
In our study, consistent with our expectation that eye
gaze would facilitate microsaccadic responses opposite
to the gaze, the microsaccade direction in the reboundphase (i.e., 400–600 ms relative to the onset of facial
stimulus presentation) was biased to the direction opposite to the gaze, regardless of facial expression. With
regard to intrinsic covert attention caused by cues presented in the visual field center that imply the directionof target appearance, the generated microsaccades arebiased in the cue-indicated direction [7]. By contrast,with regard to exogenous attention automatically generated by cues presented around the visual field, microsaccades are biased in the opposite direction of the cues
[15, 18]. Previous studies [7, 15, 18] have reported thesemicrosaccade biases in the rebound phase (i.e., 200–
600 ms relative to the stimulus onset of a directional cue
presentation). This phenomenon can be explained by the“inhibition hypothesis” [20]. In this experiment, the participants were required to maintain a central fixation andrequired to suppress reflexive saccade movements due togaze perception [27]. This saccade inhibition may havecaused bias in the opposite direction.
A contradiction exists between our findings and the“IOR hypothesis” [17], which is the interpretation of
microsaccade bias in opposite directions. A previous
study [75] directly compared the automatic attention

orientation of social cues (i.e., gaze) and nonsocial cues
(i.e., peripheral cues) and reported that the social cues
did not cause IOR. This finding suggests that the importance of social information negates the subcortical mechanisms underlying IOR [75]. Our findings regarding RT
confirmed that attention was facilitated in the gaze direction and did not show IOR (Table 1). Nevertheless, themicrosaccades were biased in the direction opposite to
the gaze direction in the rebound phase (Fig. 4). These
results support that microsaccades could be biased to the
opposite direction of spatial attention induced by other’s gaze without IOR, which indicates that IOR may beinsufficient to explain the opposite microsaccade directional bias.
Of note, our findings support that eye gazes, as well
as spatial cues eliciting exogenous attention, biased themicrosaccadic direction opposite to the direction of spatial attention. However, the contradiction between our
results and the IOR hypothesis suggesting that microsaccadic directional bias by others’ gaze could not be
fully explained by the theory on exogenous attention.
We speculate that attentional orientation automaticallyinduced by eye gaze may involve a more complex neuralnetwork for social cognition. This idea is consistent with
one proposed in a previous review [29] and should be
examined in the future.
With regard to the effects of facial expression on the
microsaccadic directional bias, contrary to the reboundphase (i.e., 400–600 ms relative to the onset of facial
stimulus presentation) in which extensive studies havereported microsaccade bias, the microsaccade direction
within the interval from 800–1000 ms relative to theonset of facial stimulus presentation revealed a facialgaze interaction effect. Moreover, inconsistent with
our expectation, we observed significant microsaccadic
directional bias opposite to the gaze within this phasein the neutral conditions but not in the fear condition(Fig. 5). An increase in the microsaccade rate in the same
direction was also observed in the fear condition compared to the neutral condition (Fig. 5). In both "inhibition of return" and "inhibition hypothesis", microsaccadebiases suppress saccades in the same direction as thespatial attentional direction induced by the cue stimulus.
Thus, our results suggest that the directional bias, accompanied by the suppression of microsaccades in the same
direction as eye gaze, was observed to disappear during
the 800–1000 ms time period in the fear condition. Eyegaze with a fearful facial expression is a social stimulusthat implies a threat toward the direction of the gaze.
Shortening the duration of spatial attention toward theimplied threat, rather than sustaining spatial attention,

Motomura et al. Journal of Physiological Anthropology(2023) 42:19

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may be advantageous in survival and immediate actions(e.g., fleeing). We speculate that the disappearance of the
microsaccadic directional bias for eye gaze with fearfulexpression in the temporally late phases will be associated with such adaptive responses in spatial attention forpotential threats, which should be examined in futurestudies.
This finding suggested that the microsaccadic responseto the gaze-mediated attention shift is differentiallymodulated, based on cognitive processing of the facial
expression associated with the gaze. Together with theaforementioned results (post-presentation interval from
400 to 600 ms), this finding suggested that the microsaccadic response may reflect social cognitive processing.
The mechanism underlying this phenomenon remains
unclear; however, the microsaccadic response could
reflect an individual’ s attentional traits. In this study,
we conducted exploratory correlation analysis to preliminarily investigate the association between microsaccade response and an individual’s attentional trait. The
results suggested that low microsaccadic responses (i.e.,the microsaccade rate and microsaccade directional
bias score) in the interval of 800–1000 ms relative to theonset of a gaze with fearful expression were associatedwith inattentive tendencies (CAARS subscale A: inattention/memory problems) (Table 3 and Fig. 6). This finding
indicated that the microsaccadic response to perceiving other’s gaze with their facial expressions may reflectattentional function, possibly associated with an impairment pattern of inattention in ADHD.
Studies have indicated that patients with ADHD have
deficits in oculomotor control. Previous studies havereported that, compared to typically developing individuals, individuals with ADHD have a lower ability to maintain fixation [76] and suppress inappropriate saccades[77]. Compared to neutral expressions, fearful expressions enhance attention to the gaze direction [60, 62–66];
therefore, they involve greater difficulty [27] in suppressing saccades induced by gazes with fearful expressions.
Such difficulties in suppressing saccades and maintaining
fixation may cause low microsaccade rates, because themicrosaccade occurs during fixation [1, 2]. Additionally,
the inhibition hypothesis [20] suggests that difficulties
in suppressing saccades and in maintaining fixation areassociated with attenuated microsaccadic directional bias
opposite to the direction of the spatial attention. Thesefindings suggested that individuals with a high ADHD
tendency may be more strongly distracted to gaze cues offearful facial expressions, and therefore may not be able
to maintain fixation and may have lower microsaccade
responses during fixation. With regard to the attentionfunction in individuals with ADHD, evidence for a close
relationship between attention and oculomotor control

mechanisms [70] in psychological, functional anatomical, and cellular levels [78] suggests that the inattentional
properties of ADHD could involve inhibitory deficits
in ocular motor behavior [79]. Our findings support
this concept; moreover, our study is the first to indicatethat the features underlying eye movement inhibition in
ADHD may be shown as a microsaccade bias toward spatial attention.
Some limitations require acknowledgment. First,
we only used the fearful face of an unknown person asa social signal, which is an important social cue implying that fearful objects exist in the line of sight. Second,
our findings suggesting an association of microsaccadic
responses to others’ gaze with ADHD tendencies are
preliminary. Additionally, the participants were limited
to healthy young men without an ADHD diagnosis. In
future studies, these findings should be tested by using
other populations, including individuals with neurodevelopmental disorders such as ADHD.

Conclusions
We examined the effect of others’ gaze on the observer’s
microsaccades. First, we found that conscious perception of others’ gaze guided the observer’s attention andmicrosaccade biases in the opposite direction of the gaze.
These biases showed different modulations, dependingon the cognitive processing of the facial expressions of
the gaze. In particular, microsaccade bias in gazes withfearful facial expressions may reflect ADHD-relatedcharacteristics. This finding suggested that microsaccade
modulation by cognitive gaze processing may reflect theneural mechanisms underlying the ADHD characteristics
such as inattention.
Our findings suggested that microsaccades areassociated with social cognitive processing, as well
as attention and emotional processing, which may
contribute to the development of a theory regarding
microsaccades function in social cognition. Microsaccade studies on social cognition may help elucidate thepathophysiological responses to psychiatric disorders,
including ADHD. Therefore, our findings further indicate the utility of microsaccades as biomarkers for an
ADHD diagnosis.
Abbreviations
ADHD	Attention-deficit/hyperactivity disorder
ANOVA	Analysis of variance
CAARS	Conners’ Adult ADHD Rating Scale
DSM-IV	
Diagnostic and Statistical Manual of Mental Disorders, Fourth
Edition
IOR	Inhibition of return
RT	Reaction time
SOA	Stimulus-onset asynchrony

Motomura et al. Journal of Physiological Anthropology(2023) 42:19

Supplementary Information
The online version contains supplementary material available at https://​doi.​
org/​10.​1186/​s40101-​023-​00335-2.
Additional file 1: Supplementary Figure 1. Eye movements and microsaccade detections during fixation. Supplementary Figure 2. Average
microsaccadic rates and the function of detection threshold λ. Supplementary Figure 3. Relationship between the peak velocity and the amplitude of detected microsaccades and their histograms.
Acknowledgements
We appreciate the time and effort spent by our participants. We would like tothank Editage (www.​edita​ge.​com) for English language editing.
Authors’ contributions
RK and YM designed the experiment. RK and YH performed experiment. RK
analyzed the data with advice from YM and SHi. YM and SHa wrote the manuscript with useful discussion with all authors. TO revised the manuscript from aclinical perspective. All authors read and approved the final manuscript.
Funding
This research was supported by the operating expenses for Kyushu University
departments, JSPS Grant-in-Aid for Scientific Research (19K16244), and AMED
under grant number JP19ak0101059.
Availability of data and materials
The datasets generated during and/or analyzed during the current study areavailable from the corresponding author on reasonable request.

Declarations
Ethics approval and consent to participate
This study was approved by the Research Ethics Committee of Kyushu
University (Fukuoka, Japan). Written informed consent was obtained from allparticipants.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Received: 26 September 2022 Accepted: 26 July 2023

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