Neuropsychologia 51 (2013) 1161–1168

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Neuropsychologia
journal homepage: www.elsevier.com/locate/neuropsychologia

Unconscious processing of direct gaze: Evidence from an ERP study

Takemasa Yokoyama a,b,n, Yasuki Noguchi a, Shinichi Kita a
a
Departiment of Psychology, Kobe University, Kobe, Japan
b
Japan Society for the Promotion of Science, Tokyo, Japan

art ic l e i nf o a b s t r a c t

Article history: Humans detect faces with direct gaze more rapidly than they do faces with averted gaze. Evidence
Received 31 July 2012 suggests that the visual information of faces with direct gaze reaches conscious awareness faster than
Received in revised form that of faces with averted gaze. This suggests that faces with direct gaze are effectively processed in the
20 March 2013
brain before they reach conscious awareness; however, it is unclear how the unconscious perception of
Accepted 1 April 2013
faces with direct gaze is processed in the brain. To address this unanswered question, we recorded event-
Available online 17 April 2013
related potentials while observers viewed faces with direct or averted gaze that were either visible or
Keywords: rendered invisible during continuous flash suppression. We observed that invisible faces with direct gaze
Direct gaze elicited significantly larger negative deflections than did invisible faces with averted gaze at 200, 250,
Interocular suppression
and 350 ms over the parietofrontal electrodes, whereas we did not observe such effects when facial
Unconscious
images were visible. Our results suggest that the visual information of faces with direct gaze is preferen-
Event-related potentials
Conscious awareness tially processed in the brain when they are presented unconsciously.
& 2013 Elsevier Ltd. All rights reserved.

1. Introduction
Eye gaze of a conspecific conveys rich signals to an observer.
Thus, gaze plays a critical role in visual processing of a face.
Research on gaze perception deals mainly with two types of gaze:
averted gaze, which is not directed at the observer, and direct
gaze, which is directed at the observer. These two types of gaze
have different effects on the perception and cognition of observers.
This functional dissociation between faces with direct and
averted gaze is typically seen in their influences on attention of
observers. It is well known that faces with direct gaze give more
salient visual signals to observers than do faces with averted gaze;
thus, faces with direct gaze are more likely to capture the spatial
attention of observers compared with averted gaze (Senju &
Johnson, 2009; Yokoyama, Ishibashi, Hongoh, & Kita, 2011). In a
visual search task, faces with direct gaze among faces with averted
gaze are detected faster and more accurately than faces
with averted gaze among faces with direct gaze (Conty, Tijus,
Hugueville, Coelho, & George, 2006; von Grunau & Anston, 1995).
On the other hand, faces with averted gaze shift the observer's
spatial attention to the direction indicated by the averted gaze. In a
gaze-cuing paradigm, observers can respond to a target more
quickly when faces with averted gaze in the center of the display
indicate a peripheral location of the upcoming target than when
n
Corresponding author at: Kobe University, Department of Tokyo, 1-1 Rokkodai-
cho, Nada-ku, Kobe, Hyogo 657-8501 Japan. Tel./fax: +81 78 803 5562.
E-mail address: yokoyama@lit.kobe-u.ac.jp (T. Yokoyama).
they do not (Friesen & Kingstone, 1998; Langton, Watt, & Bruce,
2000; Vecera & Rizzo, 2006; Yokoyama, Noguchi, & Kita, 2012).
Therefore, faces with direct gaze capture the attention of obser-
vers, whereas faces with averted gaze shift the observer's attention
to the direction indicated by the averted gaze.
Because the processing of faces with direct and averted gaze
are functionally different, the neural processing of these two types
of gaze is dissociated in the brain. Neuroimaging studies indicate
that the processing of faces with direct gaze is more closely
associated with the fusiform gyrus, right superior temporal sulcus
(STS), medial prefrontal cortex, and amygdala than the processing
of faces with averted gaze (Calder et al., 2002; George, Driver, &
Dolan, 2001; Kampe, Frith, & Frith, 2003; Kawashima et al., 1999;
Pageler et al., 2003; Pelphrey, Viola, & McCarthy, 2004; Sato,
Yoshikawa, Kochiyama, & Matsumura, 2004; Wicker, Perrett,
Baron-Cohen, & Decety, 2003). In contrast, the processing of faces
with averted gaze is related to the left STS and intraparietal sulcus
(Hoffman & Haxby, 2000; Wicker, Michel, Henaff, & Decety, 1998).
Hence, faces with direct and averted gaze are different not only
regarding behavior, but also regarding how they are processed in
the observer's brain.
Regarding the unconscious perception of faces with direct gaze,
Stein, Senju, Peelen, and Sterzer (2011) used continuous flash
suppression (CFS) to examine whether faces with direct or averted
gaze were more effectively processed without conscious aware-
ness. Those authors used CFS to render facial images invisible at
the beginning of the trials, and then ramped up the contrast of
those images until participants were consciously aware of them.
It was found that participants became aware of faces with direct

0028-3932/$ - see front matter & 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.neuropsychologia.2013.04.002
1162 T. Yokoyama et al. / Neuropsychologia 51 (2013) 1161–1168
gaze faster than they became aware of faces with averted gaze.
Therefore, the authors concluded that faces with direct gaze were
effectively processed without conscious awareness, which implies
that these faces gain preferential access to the conscious aware-
ness of faces.
Although Stein et al. (2011) study suggested that invisible faces
with direct gaze induced stronger neural responses compared
with faces with averted gaze, little is known about the uncon-
scious neural processing of faces with direct gaze in the brain. To
address this, we used electroencephalography (EEG) and recorded
event-related potentials (ERPs) evoked by images of faces with
direct gaze rendered invisible through CFS. Our aim was to identify
the neural correlate of increased sensitivity to invisible faces with
direct gaze compared with averted gaze. The high temporal
resolution of EEG enabled us to measure the speed at which the
invisible gaze information reached different parts of the brain.
2. Experiment 1 (behavioral experiment)
Before performing the EEG experiments, we replicated the
study of Stein et al. (2011) to confirm that the preferential
processing of faces with direct gaze relative to averted gaze also
occurred in our study.
2.1. Methods
2.1.1. Participants
Five participants (three men and two women; age range, 20–31
years) were recruited from the Psychology Department of Kobe
University. Informed consent was received from each participant
after the nature of the study had been explained. All participants
had normal or corrected-to-normal acuity of vision and had no
history of neurological diseases. All individuals were naïve to the
purposes of this experiment. Approval for the experiment was
obtained from the ethics committee of Kobe University, Japan.
2.1.2. Stimuli and procedure
Visual stimuli were displayed on a Sony MultiScan 17sf II
14.1 in. CRT display with a resolution of 1024
768 pixels. Displays
and data collection were controlled with MATLAB using the
Psychophysics toolbox (Brainard, 1997; Pelli, 1997) on a Dell
Optiplex 360 computer running Microsoft Windows XP (refresh
rate, 60 Hz).
To create dichoptic viewing, we presented stimuli at two
different locations on the screen. Two white frames (6.1
6.11)
were displayed side by side on the screen, with one frame
presented to each eye. A mirror stereoscope fused stimuli at those
two locations. We used four pictures of faces (two males and two
females) from the ATR DB99 database (ATR-Promotions, Kyoto,
Japan). The gaze direction of each pictured person was leftward,
straight, and rightward. The overall luminance and contrast levels
of all pictures were adjusted using MATLAB. After controlling the
luminance and root mean square (RMS) contrast levels, we
performed an analysis of variance (ANOVA), which indicated the
absence of significant differences between direct-gaze, rightward-
gaze, and leftward-gaze pictures regarding luminance levels
(F2,11 ¼ 0.019, p ¼0.9815, n.s.) or RMS contrast levels (F2,11 ¼ 0.500,
p ¼0.6224, n.s.). The mean and standard error values of luminance
and RMS contrast are presented in Table 1A. Direct-gaze pictures
were used for the direct-gaze condition, and leftward- and
rightward-gaze pictures were used for the averted-gaze condition.
In the averted-gaze condition, images of leftward gaze were
positioned in the upper-left corner of the frame, whereas images
of rightward gaze were positioned in the upper-right corner of
the frame.
Table 1A.
Mean and standard deviation of luminance and RMS contrast in Experiment 1
(behavioral experiment).
Direct gaze Rightward gaze Leftward gaze
Mean s.d. Mean s.d. Mean s.d.
Luminance 14.350 0.555 14.425 0.531 14.422 0.533
Contrast (RMS) 5.000 0.000 4.997 0.004 4.997 0.004
(cd/m2)
The experiment used a one-factor repeated-measure design
with two levels of gaze direction: direct and averted gaze. An
experimental block consisted of 80 trials, in which the two
conditions were intermixed randomly. Ten practice trials preceded
the experimental trial.
Fig. 1A shows an example of a trial sequence. Each trial cycled a
fixation display (1000 ms) as a preflash period; this was followed by
the presentation of a rapid sequence of high-contrast colored
Mondrian patterns at 20 Hz to the dominant eye of the participant.
The colored Mondrian patterns were used as continuous flashes that
rendered low-contrast images invisible (Noguchi, Yokoyama, Suzuki,
Kita, & Kakigi, 2012; Stein, Peelen, & Sterzer, 2012; Tsuchiya & Koch,
2005). To determine eye dominance in participants, we used a
variation of the Porta test (Roth, Lora, & Heilman, 2012); three
participants had dominant right eyes. Conversely, a facial image
was gradually introduced to the nondominant eye, and the contrast
of the facial image was ramped up linearly from 0% to 100% over 1 s.
Facial images appeared either at the upper-left or upper-right corner
of the white frame. The continuous flashes and facial images were
presented until participants responded, or for 10 s. Participants
pressed the left or right key as quickly and accurately as possible
when any part of the facial image became visible.
2.2. Results
Fig. 1B shows the mean reaction time of the two gaze-direction
conditions. A t test analysis revealed the presence of a significant
difference between the two conditions (t4 ¼−3.438, p o0.05). This
result provides evidence that the preferential processing of faces
with direct gaze, compared with faces with averted gaze, occurred
in our study. Based on our behavioral results, we measured ERPs to
investigate the neural mechanisms underpinning the enhanced
sensitivity to process unconsciously faces with direct gaze.
3. Experiment 2 (EEG experiment)
3.1. Methods
The method described in Experiment 2 was similar to that used
in Experiment 1, with the exception of the following details.
3.1.1. Participants
Twelve participants (nine men and three women; age range,
20–29 years) were recruited from the Psychology Department of
Kobe University. Informed consent was received from each parti-
cipant after the nature of the study had been explained. All
participants had normal or corrected-to-normal acuity of vision
and had no history of neurological diseases. All individuals were
naïve to the purposes of this experiment. Approval for the
experiment was obtained from the ethics committee of Kobe
University, Japan.
 T. Yokoyama et al. / Neuropsychologia 51 (2013) 1161–1168
Fig. 1. A trial sequence and the results in the Experiment 1. (A) An example of the
sequence of events in a typical trial in the Experiment 1. A facial image (direct or
averted gaze) and colored Mondrian pattern were presented to non-dominant and
dominant eye, respectively. Those images were fused by a mirror stereoscope. A
contrast of a facial image was gradually ramped up, and participants judged
whether a facial image appeared at upper left or upper right of the frame.
(B) Results in the Experiment 1. The horizontal axis indicates reaction time that
participants responded to averted gaze(s), and the vertical axis indicates reaction
time that participants responded to direct gaze(s). All participants (n¼ 5)
responded to direct gaze more quickly than averted gaze.
3.1.2. Stimuli and procedure
We used six pictures (three men and three women) from the ATR
DB99 database (ATR-Promotions, Kyoto, Japan), and gaze direction
was leftward, straight, and rightward for each pictured person. To
create visible and invisible conditions, we prepared high- and low-
contrast pictures. The overall luminance and contrast levels of the
pictures were adjusted using Adobe Photoshop 6.0 for both high- and
low-contrast pictures. After controlling the luminance and RMS
contrast levels, we performed ANOVA, which indicated the absence
of significant differences between direct-gaze, rightward-gaze, and
leftward-gaze pictures regarding luminance levels (F2,17 ¼0.065,
p¼0.9375, n.s.) or RMS contrast levels (F2,17 ¼ 1.519, p¼ 0.2508, n.s.)
for high-contrast pictures, and absence of significant differences
between direct-gaze, rightward-gaze, and leftward-gaze pictures
regarding luminance levels (F2,17 ¼0.207, p¼0.8154, n.s.) or RMS
contrast levels (F2,17 ¼0.341, p¼ 0.7162, n.s.) for low-contrast pictures.
1163
Table 1B.
Mean and standard deviation of luminance and RMS contrast in high-contrast and
low-contrast pictures in Experiment 2 (EEG experiment).
Direct gaze Rightward gaze Leftward gaze
Mean s.d. Mean s.d. Mean s.d.
High-contrast pictures
Luminance 26.528 0.099 26.542 0.141 26.590 0.126
Contrast (RMS) 14.564 0.080 14.558 0.075 14.604 0.059
Low-contrast pictures
Luminance 8.780 0.192 8.735 0.302 8.690 0.217
Contrast (RMS) 1.525 0.036 1.518 0.016 1.511 0.027
(cd/m2)
The mean and standard error values of the luminance and RMS
contrast are presented in Table 1B.
Fig. 2 shows an example of a trial sequence. Each trial cycled
through a fixation display (1000 ms) as a preflash period, followed
by the presentation of a rapid sequence of high-contrast colored
Mondrian patterns to the dominant eye of the participant. To
determine eye dominance in participants, we used a variation of
the Porta test (Roth et al., 2002). All participants had dominant
right eyes. Each colored Mondrian pattern appeared for 50 ms, 26
different patterns were used in each trial, and the duration of the
flash period was 1300 ms. Conversely, the images presented to the
nondominant eye differed depending on seven types of trials
that were intermixed randomly: high-contrast direct gaze, high-
contrast rightward gaze, high-contrast leftward gaze, low-contrast
direct gaze, low-contrast rightward gaze, low-contrast leftward
gaze, and gray trials. Stimuli were presented to the nondominant
eye for 500 ms. In the high-contrast conditions, participants
perceived the gaze direction of the target faces consciously
because of the high luminance contrast of those images. In the
low-contrast conditions, however, the luminance contrast of the
facial images was too low for them to be perceived consciously
under CFS. In the gray trials, no images were presented throughout
the flash period. The duration of the presentation of all images to
the nondominant eye was between 600 and 1100 ms after the
onset of the continuous flashes; thus, neural responses to the facial
images were not confounded with those induced by the onset
of continuous flashes. Subsequently, we presented continuous
flashes to the nondominant eye in the last 200 ms of each trial
to prevent the perception of afterimages.
After the trials, participants were required to answer two
questions sequentially. The first question probed target detection
(subjective measurement): participants pressed one key when
images were visible and another key when images were invisible.
The second question probed the participants’ ability to identify
accurately the gaze direction of facial images (objective measure-
ment). Even if participants answered “no” to the first question, the
second question was presented to exclude the possibility of the
unconscious processing of invisible stimuli. An experimental
block consisted of 84 trials in which the seven conditions (12
trials for each condition) were intermixed randomly. Six blocks
were conducted.
3.1.3. EEG measurement and data analysis
EEG was recorded from 19 scalp electrodes (FP1, FP2, F3, Fz, F4,
F7, F8, C3, Cz, C4, T3, T4, T5, T6, P3, Pz, P4, O1, and O2) (EEG1200;
Nihon Koden, Tokyo, Japan). EEG was recorded continuously at a
rate of 500 Hz and referenced with an average potential measured
from the right and left earlobes. Neural activity in response to the
facial images was examined by measuring visual-evoked poten-
tials (VEPs) that were time locked to the onset of those images. We
1164 T. Yokoyama et al. / Neuropsychologia 51 (2013) 1161–1168

epoched and averaged EEG waveforms ranging from −700 to results of tasks 1 and 2 suggest that the CFS blocked the
500 ms relative to the onset of the facial images. EEG signals in a conscious perception of the low-contrast facial images, whereas
period of −50 to 0 ms were used as a baseline. Epochs with signal the high-contrast facial images broke the CFS and were processed
variations exceeding 100 μV were excluded from the analysis. consciously.
Finally, VEPs were band-pass filtered at 0.5–30.0 Hz. Because some
participants reported conscious detection of the low-contrast
facial images during CFS in a small portion of trials, EEG wave-
forms in such trials were eliminated from the analysis, to ensure
the quality of unconsciousness.

3.2. Results

3.2.1. Behavioral data

Fig. 3A shows the behavioral results of task 1 (detection task)
averaged across the 12 participants. The mean ( 7 SE across
participants) detection rates for the high-contrast pictures were
99.7 7 0.2% (high-contrast direct gaze), 98.1 7 0.3% (high-contrast
rightward gaze), and 99.6 7 0.3% (high-contrast leftward gaze).
This result indicates that participants were able to detect the
high-contrast facial images even during CFS. Conversely, the
detection rates for the low-contrast pictures were 0.9 7 0.5%
(low-contrast direct gaze), 0.9 7 0.4% (low-contrast rightward
gaze), and 0.7 7 0.3% (low-contrast leftward gaze), which were
comparable to the false-alarm rates recorded in the gray condi-
tion (0.7 7 0.3%), in which no facial image was presented. We
performed one-way ANOVA to test for the presence of significant
differences between detection rates in the low-contrast condi-
tions and false-alarm rates in the gray condition. There were no
significant differences between the low-contrast direct gaze, low-
contrast rightward gaze, low-contrast leftward gaze, or gray
condition (F3,47 ¼0.169, p ¼0.9167). Thus, the detection rates in
the low-contrast conditions and false-alarm rates in the gray
condition were not significantly different. These data indicate
that participants could not consciously perceive the low-contrast
images regardless of whether gaze direction was direct, right-
ward, or leftward. Subsequently, we used a gaze direction
discrimination task to confirm that the low-contrast images were Fig. 3. Behavioral results of tasks 1 and 2. All error bars denote standard errors
invisible to participants (Fig. 3B). The accuracy of the high- (SEs). (A) Results of task 1 (detection task). The presentation of facial images with
contrast condition was almost 100% (98.3 7 0.1%), which was direct, rightward, and leftward gazes with a high luminance contrast during the
continuous flashes broke the suppression and came into the consciousness of
significantly higher (t11 ¼190.1, p o 0.001) than the chance level
participants. In contrast, almost all facial images of direct, rightward, and leftward
(33.3%). In contrast, the accuracy of the low-contrast condition gaze with a low luminance contrast were invisible throughout the trial. We set the
was 34.3 7 1.8%, which was not significantly different from the gray condition, in which no facial image was presented, as a control. False-alarm
chance level (t11 ¼0.34, p ¼0.73). To test that observers were not rates in the condition were comparable to the detection rates observed in the low-
able to discriminate the gaze direction of facial images in the contrast conditions. (B) Results of task 2 (discrimination task). The mean accuracies
in the high-contrast and low-contrast conditions were 98.3% and 34.3%, respec-
low-contrast conditions, we performed ANOVA to compare the tively. There were no significant differences between the low-contrast conditions
three low-contrast conditions and found no significant differ- and the chance level (33.3%), which indicates that facial images presented in low-
ences between the three conditions (F2,35 ¼1.194, p ¼0.321). The contrast conditions were totally suppressed during the flash period.

Fig. 2. An example of the sequence of events in a typical trial. Two different images were presented to the dominant and nondominant eyes of participants and a mirror
stereoscope fused those images. After the presentation of a fixation screen for 1 s, continuous flashes of 20 Hz were given to the dominant eye, which rendered a target facial
image invisible to the nondominant eye. After presentation of continuous flashes, participants were required to perform two tasks: detection and discrimination tasks.
 T. Yokoyama et al. / Neuropsychologia 51 (2013) 1161–1168
Fig. 4. Depiction of the 19 electrode positions over the scalp and the grand-averaged ERPs evoked by high-contrast conditions (positive: upward). The zeros in the horizontal
axis denote the onset of the presentation of facial images.
3.2.2. VEP waveforms
Because no facial images were presented in the gray condition,
the ERPs induced by the gray condition should reflect neural
responses to continuous flashes, not faces. To isolate the ERP
components related to gaze perception, we subtracted EEG wave-
forms in the gray condition from those of the other gaze condi-
tions. We separated the high-contrast conditions from the low-
contrast conditions to investigate VEPs from the 19 points on each
participant's scalp. Fig. 4 shows the grand-averaged VEPs at all 19
electrodes for the high-contrast conditions, and Fig. 5 shows the
grand-averaged VEPs at all 19 electrodes for the low-contrast
conditions. Some studies have suggested that, compared with
faces with averted gaze, faces with direct gaze elicit a larger N1
in the posterior channels, such as O1, O2, T5, and T6 (Conty,
N'Diaye, Tijus, & George, 2007; Pesciarelli, Sarlo, & Leo, 2011) when
the two types of gaze are presented consciously. Thus, we
averaged the EEG waveforms in the high-contrast conditions
across the four electrodes listed above, and applied one-factorial
repeated-measures ANOVA to the averaged ERP amplitude within
a 150–230 ms latency range (Taylor, George, & Ducorps, 2001). This
analysis revealed an absence of significant main effects between
the three conditions (F2,35 ¼ 0.353, p¼ 0.7068). In contrast, regard-
ing the unconscious processing of face stimuli, previous studies
reported a negative deflection of EEG signals to faces presented
unconsciously between 200 and 300 ms after stimulus onset
(Liddell, Williams, Rathjen, Shevrin, & Gordon, 2004). Consistent
with this report, we observed in some electrodes that the ERP
components of the low-contrast direct-gaze condition were larger
than the ERP components of the low-contrast rightward- and
leftward-gaze conditions at 200–300 ms. To analyze those compo-
nents selective to direct gaze statistically, we first averaged the
1165
data of the low-contrast rightward- and leftward-gaze conditions,
making ERPs in the averted-gaze condition as a control. Subse-
quently, we performed a t test analysis at each channel to explore
which channels exhibited significant differences between direct
and averted gaze in the invisible conditions. There were significant
differences between direct and averted gaze at F4 (t11 ¼ −2.23;
po 0.05), C4 (t11 ¼−2.46; p o0.05), Fz (t11 ¼−2.25; p o0.05), and
Cz (t11 ¼−2.26; p o0.05) (see gray-shaded windows in Fig. 5). The
responses at those electrodes are enlarged in Fig. 6A. We then
created 50 ms time windows (Fig. 6B) and performed 2 (direct/
averted: gaze direction)
4 (channel)
8 (time window) repeated-
measures ANOVA. We found significant main effects of gaze
direction and time window (F1,714 ¼ 11.545, po0.001 for gaze
direction; F7,714 ¼3.661, po0.001 for time window), but not
of channel (F3,714 ¼ 0.171, p¼0.916). The interaction between gaze
direction and time window was significant (F7,714 ¼2.109, po0.05);
however, we did not find a significant interaction between gaze
direction and channel (F3,714 ¼ 0.426, p¼ 0.735) or between channel
and time window (F21,714 ¼0.180, p¼1.000). Because the main
effects of channel and interactions including channel were not
significant, we factored out the effects of channel and performed
two-way ANOVA (gaze direction and time window). There were
significant main effects of gaze direction (F1,741 ¼ 11.889, po0.001)
and time window (F7,741 ¼3.770, po0.001), and a significant
interaction between gaze direction and time window (F7,741 ¼
2.172, po0.05). To examine which of the time windows exhibited
significant differences between direct and averted gaze, we performed
a post hoc analysis of interaction using a Bonferroni correction.
There were significant differences between direct and averted
gaze at time windows of 200 ms (corrected p o0.005), 250 ms
(corrected po 0.001), and 350 ms (corrected po 0.05) (Fig. 6C).
1166 T. Yokoyama et al. / Neuropsychologia 51 (2013) 1161–1168

Fig. 5. Depiction of the 19 electrode positions over the scalp and the grand-averaged ERPs evoked by the low-contrast conditions (positive: upward). The zeros in the
horizontal axis denote the onset of the presentation of facial images. Specific responses for direct gaze only were observed in the four parietofrontal channels (Fz, F4, Cz, and
C4; green circles). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

4. Discussion Why did we obtain differential responses to direct vs. averted

This study was the first to investigate the neural correlate of
increased sensitivity to the unconscious processing of faces with
direct gaze. We recorded EEG during CFS to address this question.
The effect of the unconscious perception of faces with direct gaze
appeared at time windows of 200, 250, and 350 ms after stimulus
onset at the parietofrontal electrodes. No specific neural responses
to invisible faces with direct gaze were observed at the occipital or
temporal electrodes, which might be consistent with previous
findings reporting a lack of aftereffects induced by invisible faces
with direct gaze (Stein et al., 2012). Taken together, our findings
suggest that faces with direct gaze are processed effectively under
an unconscious condition, and that this effect occurs 200, 250,
and 350 ms after the unconscious representation of faces with
direct gaze.
Previous studies found large negative deflection at 200–300 ms
at the parietofrontal electrodes when fearful faces were presented
subliminally (Kiss & Eimer, 2008; Liddell et al., 2004). The large
EEG waveforms observed in these studies are similar to our
waveform data of faces with direct gaze. Given that the presenta-
tion of fearful faces and faces with direct gaze evokes emotional
responses in observers (Pessoa & Adolphs, 2010; Senju & Johnson,
2009), the EEG components of 200–300 ms in response to faces
with direct gaze observed in the present study might reflect
unconscious emotional responses. Our data clearly demonstrated
a latency of the processing of unconscious faces with direct gaze,
but did not reveal the brain regions that were related to the
processing; thus, additional neuroimaging studies are necessary to
elucidate the specific brain regions that are mainly associated with
the processing unconscious faces with direct gaze.
gaze in the invisible condition only? One possibility is the
involvement of feedback neural signals that are uniquely induced
by visible stimuli. Feedback neural signals are neural activations
that are essential for visual awareness (Dehaene, Changeux,
Naccache, Sackur, & Sergent, 2006; Lamme, 2003). Although the
conscious perception of visual stimuli evokes brain responses that
are distributed widely across the entire brain, those strong
responses sometimes mask subtle differences among conditions.
For instance, Jiang and He (2006) used functional magnetic
resonance imaging to compare the neural responses to neutral
and fearful faces that were either visible or rendered invisible by
CFS. In the visible (no CFS) condition, those authors found
significant hemodynamic responses in the STS to both neutral
and fearful faces. In contrast, under the invisible condition, the
same STS region indicated a significant response only to fearful
faces. Because the fusiform face area (FFA) was similarly activated
by the invisible neutral and fearful faces, the overall result
obtained in the invisible condition indicates a clear functional
distinction between the FFA (structural encoding) and STS (expres-
sional or emotional analyses). Jiang and He (2006) concluded that
this clear distinction was caused by an absence of awareness of
facial information, which minimized the cortical responses asso-
ciated with the conscious perception of faces.
We suggest that significant responses to invisible faces with
direct compared with averted gaze can be explained by a lack of
consciousness-related activity under unconscious conditions. In
fact, the results of previous neurophysiological studies that inves-
tigated the effect of visible direct and averted gaze are incon-
sistent. Some studies have suggested that faces with direct gaze
evoked larger VEPs than did faces with averted gaze (Conty et al.,
 T. Yokoyama et al. / Neuropsychologia 51 (2013) 1161–1168 1167

Fig. 6. EEG waveforms and time sequence at four channels. (A) EEG waveforms of direct gaze and averted gaze. Averted-gaze data were created by averaging low-contrast
rightward and leftward gaze data. (B) Mean amplitude of EEG responses over time. EEG waveforms from 0 to 400 ms were divided into eight time windows of 50 ms and the
mean amplitude within each time window was plotted as a function of time. (C) Average across four channels in panel B. Amplitude of direct gaze was more negatively
deflected than amplitude of averted gaze at time-window of 200, 250, and 350 ms after stimulus onset (*p o .05, **p o .005, ***p o.001).

2007; Senju, Tojo, Yaguchi, and Hasegawa, 2005), whereas other
studies found the opposite effects (Puce, Smith, & Allison, 2000;
Watanabe, Miki, & Kakigi, 2002). Another group found no differ-
ences between VEPs in response to faces with direct and averted
gaze (Taylor, George, & Ducorps, 2001). The inconsistency between
previous results may be attributable to the consciousness-related
neural activity induced by visible gaze, which may have masked
the small differences between the direct- and averted-gaze
conditions. Eliminating the feedback process, therefore, might
enable us to identify the distinct processing of faces with direct
and averted gaze using EEG.
In conclusion, we demonstrated the existence of a neural
correlate of increased sensitivity to the unconscious processing
of faces with direct gaze. This effect was observed 200, 250, and
350 ms after stimulus presentation. The results of our study are
consistent with those of a previous behavioral study that indicated
1168 T. Yokoyama et al. / Neuropsychologia 51 (2013) 1161–1168
that the visual information of faces with direct gaze reached visual
awareness faster than that of faces with averted gaze. We believe
that the current study will provide important clues for the
elucidation of the neural mechanism underlying the processing
of faces with direct gaze.
Acknowledgement
We greatly thank Mr. Shintaro Kimijima (Kobe University,
Japan) for his technical supports. We also thank our laboratory
members for support in carrying out this work. This study was
supported by a grant to the first author (T.Y) from the Grant-in-Aid
for JSPS Fellows [11J02271], the second author (Y.N) from the
Gran-in-Aid for Young Scientists (A) [22680022], and the third
author (S.K) from the Strategic Information and Communications
R&D Promotion Programme (SCOPE) [101707012].
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