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Effects of subconscious and conscious
emotions on human cue–reward
association learning
Noriya Watanabe
1,2,3
& Masahiko Haruno
1,4
1
Center for Information and Neural Networks, National Institute of Information and Communications Technology, Suita, Osaka
565-0871, Japan,
2
Japan Society for Promotion of Science,
3
Graduate School of Environmental Studies, Nagoya University,
4
Japan
Science and Technology Agency.
Life demands that we adapt our behaviour continuously in situations in which much of our incoming
information is emotional and unrelated to our immediate behavioural goals. Such information is often
processed without our consciousness. This poses an intriguing question of whether subconscious exposure
to irrelevant emotional information (e.g. the surrounding social atmosphere) affects the way we learn. Here,
we addressed this issue by examining whether the learning of cue-reward associations changes when an
emotional facial expression is shown subconsciously or consciously prior to the presentation of a
reward-predicting cue. We found that both subconscious (0.027 s and 0.033 s) and conscious (0.047 s)
emotional signals increased the rate of learning, and this increase was smallest at the border of conscious
duration (0.040 s). These data suggest not only that the subconscious and conscious processing of emotional
signals enhances value-updating in cue–reward association learning, but also that the computational
processes underlying the subconscious enhancement is at least partially dissociable from its conscious
counterpart.
T
o achieve our behavioural goals, we must continuously adapt our behaviour and learn from changing
circumstances. However, the great majority of incoming signals in real-life social situations is irrelevant
to our immediate goals, and may be processed unconsciously in many situations. An intriguing question is
whether such irrelevant and subconsciously received information can affect behavioural adaptation.
Many studies report that emotional information not necessary for achieving an immediate task goal can affect
aspects of human behaviour including decision making
1
, clarity of memory
2
, and learning rates during cue-
reward association learning
3
, and that this is true even when the people are aware that the information is irrelevant
to achieving the task goal. For instance, in a cue-reward association-learning study, presentation of a task-
independent fearful face just before the reward-predicting cue accelerated the learning rates compared with
presentation of a neutral face; an enhancement effect that was not found in a similarly designed short-term
memory task
3
. However, all of these experiments employed an emotional signal that subjects could consciously
perceive, and did not account for incoming information that is processed subconsciously (e.g. the surrounding
social atmosphere such as feelings of tension in a classroom). Although shorter duration of stimulus presentation
generally induces smaller behavioural effects and neuronal responses, some studies report that subconscious
presentation of information or subconscious thought results in larger effects than does conscious counterpart
4–7
,
and can affect human behaviour in daily life
8,9
. Therefore, it is important to clarify whether and how subconscious
emotional information influences human learning.
Here, we performed a computational model-based analysis of behaviour to examine how learning of a prob-
abilistic cue-reward association is affected when emotional facial expressions are shown subconsciously or
consciously before presentation of the reward-predicting cue. We have previously found that learning was
enhanced when the duration of face presentation was long (1.0 s)
3
and thus focus here on how learning is affected
by a duration (0.027–0.047 s) that yields less recognisable faces.
Results
Facial Discrimination task. Before the main learning task, we conducted a discrimination task (n 5 91) to
estimate duration thresholds for conscious discrimination of facial expressions that were based on objective
(correct rate) and subjective (confidence scoring) measures (Figure 1a). We regarded a presentation as ‘conscious’
OPEN
SUBJECT AREAS:
CLASSICAL
CONDITIONING
EMOTION
HUMAN BEHAVIOUR
CONSCIOUSNESS
Received
25 September 2014
Accepted
22 January 2015
Published
16 February 2015
Correspondence and
requests for materials
should be addressed to
M.H. (mharuno@nict.
go.jp)
SCIENTIFIC REPORTS | 5 : 8478 | DOI: 10.1038/srep08478 1
if it was delivered above both subjective and objective thresholds, and
as ‘subliminal’ if it was lower than both thresholds. We define ‘sub-
conscious’ presentation as being at a duration between subliminal
and conscious presentations.
We conducted a series of t-tests to determine the threshold duration.
Analysis showed that performance accuracy (the correct rate, [CR])
at a duration of 0.040 s was higher than at 0.033 s (paired t-test,
t
(90)
5217.808, p , 0.001 with Bonferroni corrections [BC]), but
not for any other comparisons (0.020 s vs. 0.027 s: t
(90)
522.294,
p 5 0.360; 0.027 s vs. 0.033 s: t
(90)
5 0.982, p < 1.000; 0.040 s vs.
0.047 s: t
(90)
522.470, p 5 0.225 with BC) (Figure 1b, red; com-
parison among five durations). Additionally, although the CRs in
0.020 and 0.033 s were not different from chance level (paired t-test,
0.020 s: t
(90)
5 0.156, p < 1.000; 0.033 s: t
(90)
5 2.250, p 5 0.405
with BC), CR in 0.027 s was slightly and significantly higher than
the chance level (paired t-test, t
(90)
5 3.551, p 5 0.015 with BC)
(Figure 1b red).
Consistent with the CR analysis, the subjective confidence score
index (CSI) showed that participants discriminated facial expres-
sions when they were presented for longer than 0.040 s significantly
better than at shorter durations (0.033 s vs. 0.040 s: paired t-test,
t
(90)
5217.033, p , 0.0001 with BC) (Figure 1b black). While CSI
comparisons did not differ significantly between 0.027 s and 0.033 s
(t
(90)
522.347, p 5 0.211 with BC) or between 0.040 s and 0.047 s
(t
(90)
522.373, p 5 0.199 with BC), they did differ significantly
between 0.020 s and 0.027 s (t
(90)
5219.632, p , 0.001 with BC).
We also sorted CSIs based on task performance to confirm that
participants rated their correct trials as more certain. We found that
although CSIs at 0.020 s and 0.027 s stimulus durations did not differ
between correct and error trials (paired t-test, 0.020 s: t
(90)
5 1.577,
p < 1.000; 0.027 s: t
(90)
5 1.549, p < 1.000 with BC), they did differ at
longer durations (paired t-test, 0.033 s: t
(90)
5 6.012, p , 0.0001;
0.040 s: t
(90)
5 8.981, p , 0.0001, 0.047 s: t
(90)
5 8.564, p , 0.0001
with BC) (Supplementary Fig. S1).
These results showed that participants correctly discriminated
facial expressions with high confidence at presentation durations of
0.040 s and 0.047 s, which thus represents conscious presentations
as we defined them. In contrast, it was impossible to discriminate
facial expressions either objectively or subjectively when faces were
presented for only 0.020 s. The other two durations (0.027 s and
0.033 s) represent subconscious presentation because participants
showed similar confidence levels in correct and error trials with
better-than-random CR at 0.027-s durations, while at 0.033-s dura-
tions they could not discriminate faces objectively even with the
high CSI in the correct trials. Based on these observations, we used
0.027 s or 0.033 s for the subconscious condition and 0.040 s or
0.047 s for the conscious condition in the learning task. This defini-
tion of the subconscious and conscious conditions is similar to that
in other studies using facial expressions
10,11
.
In the learning task, each participant was randomly assigned to
one of these four durations. To rule out other possible factors affect-
ing learning performance, we assessed several individual differences
including age, sex, the time we conducted the experiment, and intel-
ligence level. We did not find any factor that was biased among the
groups (Table 1, see statistical analyses for sampling bias section).
Learning task. To examine the computational processes behind the
interaction between reward learning and subconscious/conscious
emotional processing (Figure 2a and 2b), we analysed behaviour
using a reinforcement learning model. More specifically, we esti-
mated the following four parameters. The learning rate (e) controls
reward prediction error in each trial. The exploration parameter (b)
controls how deterministically a value function leads to advanta-
geous behaviour, and reward sensitivity (d) transforms the actual
reward into a subjective reward, as the emotional stimulus can
change subjective sensitivity to reward. The last parameter is a
¥100 choice bias (b), which is a value-independent bias for choos-
ing the ¥100 option. This parameter represents the possibility that
participants were biased to choose one of the two rewards depending
on facial emotional expression, regardless of cue-reward associations.
We estimated these parameters separately for fearful or neutral
conditions (see Reinforcement learning model-based analysis). Before
the detailed analysis, we quantified the appropriateness of our statis-
tical models using Akaike information criteria (AIC) and Bayesian
information criteria (BIC). As shown in Figure 2c, the ebb model,
which includes learning rate, exploration parameter and ¥100 bias,
Figure 1
|
Task design and behavioural results for the discrimination task. (A) Two facial expressions (happy or sad) were presented sequentially with
masks. Duration of each presentation was 0.020 s, 0.027 s, 0.033 s, 0.040 s, or 0.047 s. Participants were required to determine whether the presented
expressions were the ‘‘same’’ or ‘‘different’’, and to rate their confidence level (‘‘low’’, ‘‘medium’’, or ‘‘high’’). (B) Both the correct rate (CR: red)
and confidence score index (CSI: black) (mean 6 SEM) showed that the ability to discriminate facial expression sharply increased at 0.040 s (CR, paired
t-test, t
(90)
5217.808, p , 0.001; CSI, paired t-test, t
(90)
5217.033, p , 0.001 with BC). *p , 0.05, **p , 0.01, ***p , 0.005, and ****p , 0.001
throughout the figures. This image is not covered by the [CC licence]. Photographs are from the NimStim Face Stimulus Set. Development of the
MacBrain Face Stimulus Set was overseen by Nim Tottenham and supported by the John D. and Catherine T. MacArthur Foundation Research Network
on Early Experience and Brain Development. (http://www.macbrain.org/resources.htm).
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SCIENTIFIC REPORTS | 5 : 8478 | DOI: 10.1038/srep08478 2
Figure 2
|
Task design, behavioural results, and model-based analysis of the learning task. (A) Participants were required to press a button to indicate
which reward would they expected, and eventually learned the association between particular rewards and particular cues. The duration of face
presentations was randomly assigned as 0.027 s, 0.033 s, 0.040 s, or 0.047 s for each participant. (B) An example combination of the facial expression, cue,
and reward. Each of the four cues was associated probabilistically (65%) with one of the two different reward amounts, and also with one of the two
facial expressions (fearful or neutral faces with 100% probability). (C) The results of the parameter estimation by AIC and BIC. e, b, d, b represent the
learning rate, exploration, reward sensitivity, and ¥100 bias, respectively. (D) Learning curves. Each data point represents the average of five trials. (E) ebb
model-based estimation of the learning rate, the ¥100 bias, and exploration (mean 6 SEM). Photographs are from the NimStim Face Stimulus Set.
Development of the MacBrain Face Stimulus Set was overseen by Nim Tottenham and supported by the John D. and Catherine T. MacArthur Foundation
Research Network on Early Experience and Brain Development. (http://www.macbrain.org/resources.htm).
Table 1
|
Descriptive statistics for participants in the four presentation conditions
0.027 s 0.033 s. 0.040 s. 0.047 s. Statics df p
Num. of participants 20 20 31 20 - - -
Sex ratio (Male/All) 0.80 0.65 0.74 0.60 x
2
5 0.424 3 0.935
Mean Age (SD) 22.20 21.20 21.48 21.20 F 5 1.420 3, 87 0.242
(2.66) (1.47) (1.41) (1.17)
Mean clock time (hh:mm:ss) (SD) 12:51:00 12:42:00 12:32:54 13:18:00 F 5 0.322 3, 87 0.810
(2:50:00) (2:50:52) (2:34:33) (2:27:06)
Mean university/department academic score (SD) 54.63 56.50 56.21 54.38 F 5 1.955 3, 87 0.127
(4.95) (2.78) (2.90) (3.34)
Note: Mean clock time indicates the mean time at which a participant began the experiment. Mean university/department academic score was calculated as the mean academic ranking within the university
department to which each participant belonged (the mean intelligence level across Japanese universities is standardised to 50).
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SCIENTIFIC REPORTS | 5 : 8478 | DOI: 10.1038/srep08478 3
was selected by AIC, and the eb and ebb models were comparable
using BIC (eb was slightly better). Model comparisons were highly
consistent with our previous report
3
and we used the ebb model in
subsequent analyses.
Learning curves averaged separately for each cue, irrespective of
face presentation duration (n 5 91), are shown in Figure 2d. Espe-
cially in the early stages, learning was faster for cues associated with
fearful faces and the ¥100 reward than other cues (solid red line).
To conduct a more quantitative analysis, we examined the effects of
emotion (fear vs. neutral) on each parameter of the computational
model (learning rates, ¥100 choice bias, and exploration). Consistent
with our previous report with 1.0-s face presentations
3
, we found that
the learning rate was higher in the fearful condition than in the neu-
tral condition (t
(90)
5 3.077, p 5 0.003) (Figure 2e, left). Additionally,
¥100 choice bias was negative in the fearful condition (t
(90)
524.687,
p , 0.001 with BC), and no difference was found in the exploration
parameter (t
(90)
521.552, p 5 0.124) (Figure 2e, middle and right).
The only notable difference from our previous study was that ¥100
choice bias was negative in the neutral condition (t
(90)
523.401,
p 5 0.002 with BC) (Figure 2e, middle).
Having seen that emotional face presentation modulates the learn-
ing rates and ¥100 choice bias, we then investigated how subcon-
scious presentation of emotional faces affects learning rates and the
¥100 choice bias. To achieve this, we separately computed learning
rates for each presentation duration (0.027 s: n 5 20; 0.033 s: n 5 20;
0.040 s: n 5 31; 0.047 s: n 5 20) (Figure 3a). A two-way ANOVA (2
Emotions 3 4 Presentations) showed a significant main effect of
emotion (F
(1,87)
5 13.306, p , 0.001) and no main effect of presenta-
tion duration (F
(3,87)
5 2.508, p 5 0.064). Importantly, the inter-
action between emotion and presentation duration was significant
(F
(3,87)
5 2.946, p 5 0.037), suggesting that the learning enhance-
ment provided by the fearful faces may disappear at some durations.
Therefore, we looked into the effects of emotion on the learning rate
of each presentation duration.
The learning rate differences (eF 2eN) were larger than zero in the
0.027 s (t
(19)
5 2.211, p 5 0.040), 0.033 s (t
(19)
5 2.482, p 5 0.023),
and 0.047 s (t
(19)
5 2.194, p 5 0.041) conditions, but not in the 0.040 s
condition (t
(30)
520.560, p 5 0.580). This targeted analysis revealed
a trough in the emotional enhancement effect at around 40 ms. To
interpret this result in terms of perception, we sorted the subjects
by CR scores on the discrimination task (mean 6 SE CRs, ,60%:
0.478 6 0.023; 60%–70%: 0.667 6 0.007; 70%–80%: 0.757 6 0.004;
80%–90%: 0.851 6 0.006; 90%–100%: 0.960 6 0.009) and found
that the emotional face-induced increases in learning rates was
strongest (n 5 26, eF2eN 5 0.028 6 0.011) when the participants’
CRs were 60%–70% (t
(25)
5 2.628, p 5 0.014) (Figure 3b), and the
enhancement effect disappeared at around CRs of 70%–80% (n 5 17,
eF2eN 5 0.009 6 0.005, t
(16)
5 1.655, p 5 0.117) and 80%–90%
CRs (n 5 23, eF2eN 5 0.003 6 0.009, t
(22)
5 0.341, p 5 0.736). The
increase in the learning rate caused by emotional faces started to be
discernible again at CRs of 90%–100%, although this was not statis-
tically significant (n 5 11, eF2eN 5 0.014 6 0.011, t
(10)
5 1.203,
p 5 0.257).
We conducted the same analysis for the ¥100 choice bias. A two-
way ANOVA (2 Emotions 3 4 Presentations) revealed a significant
main effect of presentation duration (F
(3,87)
5 3.287, p 5 0.024),
but not of emotion (F
(1,87)
5 0.973, p 5 0.327), or the interaction
(F
(3,87)
5 0.356, p 5 0.785). Importantly, these data demonstrate that
the trough was observed for the learning rates but not for the ¥100
bias.
Discussion
In this paper, we used a computational model-based behavioural
analysis of probabilistic cue–reward association learning to deter-
mine whether subconscious and task-independent emotional signals
affect learning. We found that the learning rate for cues paired with a
fearful face was larger than for cues paired with neutral faces, and that
this enhancement effect was significant when the face was presented
subconsciously (durations of 0.027 s or 0.033 s) and consciously
(0.047 s). However, this effect disappeared at 0.040 s. Furthermore,
not only does the effect of emotional signals on learning rates vanish
at the presentation duration of 0.040 s, but this duration also corre-
sponds to the 70%–90% CR level, validating the discontinuity of the
learning-enhancement effect. Because we did not observe this effect
in the discrimination task or in the ¥100 choice bias, it is likely to be
specific to the associative learning paradigm.
The discontinuity of the learning-rate enhancement effect might
have been caused by some malfunction in our experimental devices
for stimulus presentation. However, if this was the case, we would
expect the same problem to have occurred for the objective CRs in
the discrimination task. As we did not observe any significant per-
formance trough in Figure 1b at 0.040 s, and because almost all
Figure 3
|
Average learning rates sorted by presentation duration and correct rate. (A) Learning rates sorted by presentation durations revealed a
behavioural trough in the fearful condition at 0.040 s duration. Learning rate differences (eF2eN) for each duration were higher than zero (ts $ 2.194,
ps , 0.05), except for the 0.040 s duration (t
(30)
520.560, p 5 0.580). (B) Learning rates sorted by correct rates (CRs) in the discrimination test (upper
panel) showed that participants with 60%–70% CRs were most affected in terms of their learning rates (t
(25)
5 2.628, p 5 0.014). The lower panel refers to
the number of the participants in each CR condition.
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SCIENTIFIC REPORTS | 5 : 8478 | DOI: 10.1038/srep08478 4
participants reported that they were conscious that two facial expres-
sions were presented in the 0.040 s condition (post-experimental
questionnaire), we can rule out the possibility of an experimental
device-dependent problem. Another possibility is that the trough
resulted from some sampling bias among different groups. However,
we examined sex, age, experiment time, and academic scores (as shown
in Table 1) and did not find any difference among the groups (see
Statistical analyses for sampling bias).
One plausible explanation for the disappearance of the enhance-
ment effect is that there are two pathways for emotional signal pro-
cessing in the brain
12,13
. One system is the cortical pathway, which is
routed through several visual stages such as the retina, lateral geni-
culate nucleus of the thalamus, primary visual area cortex, higher-
order brain areas, and finally extending to the amygdala. This route
of information processing results in precise perception in which we
are conscious of presented stimuli. The other system is the subcor-
tical pathway, which is routed through the retina, superior colliculus,
pulvinar nucleus of the thalamus, and extends to the amygdala.
Although information processing via this route is comparatively
crude, it is thought to be an implicit system that works faster than
the cortical pathway. Several behavioural and brain-imaging studies
have shown that the subcortical pathway has sensitivity to the rapid
presentation (faster than 0.033 s) of emotional facial expressions
11,14,15
.
Therefore, the subconscious presentation (0.027 s and 0.033 s) of
stimuli presented here could have driven the subcortical pathway,
whereas the 0.047 s presentation drove the cortical pathway. These
two systems could have different effects on reward-based learning
systems that include the substantia nigra, ventral striatum, and amyg-
dala as implicated in previous studies
3,11,14–17
.
Similar discontinuity effects observed in behavioural responses
to visual stimuli have also been reported as the ‘performance-dip
effect
5,6
, which is defined as the lowered accuracy in a main task when
it is paired with the presentation of a para-threshold task-irrelevant
stimulus. These experiments and our current observations are com-
patible in the sense that performance of the main task was affected
when either a subconscious or clear task-irrelevant visual stimulus
was presented. Importantly however, while previous experiments
showed that the task-irrelevant stimuli reduced performance, our
results showed the opposite effect: subconscious emotional signal
enhanced learning.
One might wonder which enhances learning more, conscious or
subconscious perception of emotional stimulus. Although the effects
of subconscious stimulation tend to be weaker in general than con-
scious stimulation, some studies have reported that subconscious
presentation of stimuli was more effective
4–6
. Here, we showed that
enhancement by emotion perception was significant in both subcon-
scious and conscious conditions, except when the stimulus duration
was 0.040 s. However, as shown in Figure 3b, participants were most
affected by the emotional signal when their accuracy was between 60%
and 70%. This result seems to suggest that the learning-enhancement
effect is strongest when the emotional signal is presented obscurely.
Figure 3b also indicates that overly quick stimulus presentation
(,60% CRs: mean CR 5 0.478 6 0.023) does not enhance learning
rates. These results may indicate that there is an optimal range of
presentation durations for emotional signals that yield subconscious
enhancement of learning.
Finally, while the ¥100 choice bias (which was independent of
learning) was also affected by presentation duration, no trough in
the effect was observed. Although faces were unrelated to our main
learning task, the subconsciously presented faces may have induced
uncertainty
18
or anxiety concerning subjective perception, and the
negative feeling may have led to negative choices (smaller reward).
Such a transfer of the task-independent feeling to the main task could
well be linked with Pavlovian Instrumental Transfer (PIT)
19,20
. The
PIT is a phenomenon in which previously conditioned Pavlovian
cues affect the subjective prediction and motivation in subsequent
instrumental conditioning from the outset, despite no explicit asso-
ciation between the Pavlovian cue and the new learning
19,20
. In the
current learning experiment, the subconscious presentation of facial
expressions could have induced negative emotion, and this emotion
then transferred the subsequent associative learning from the very
first trial. Such a negative bias might have been quantified as the
negative ¥100 choice bias.
Methods
Participants. Participants in this study were undergraduate and graduate students
who did not declare any history of psychiatric or neurological disorders. All
experiments were conducted according to the principles in the Declaration of
Helsinki and were approved by the ethics committee of the National Institute of
Information and Communications Technology. All 130 participants gave informed
consent prior to the experiments. Thirty-nine people (30.0%) were unable to learn all
four of the associations. Therefore, we analysed data from the remaining 91
participants (64 male; mean age 21.5 6 1.7 years).
Experimental design. Stimuli were presented via a Dell precision T7500 computer
with a graphics accelerator (NVIDIA Quadro 4000) and 19 inch CRT display (SONY
CPD-G420) to achieve 150 Hz refresh rates. Stimulus presentation and response
acquisition were controlled using Psychtoolbox-3 software (www.psychtoolbox.org)
with MATLAB. Stimuli were presented within an area subtending 4.49 3 6.16 degrees
of visual angle.
Facial discrimination task. Prior to the learning task, all 91 participants performed
the facial expression discrimination task (Figure 1a), which measured the
presentation-time threshold for subconscious and conscious facial expression
discrimination. We used 8 happy and 8 sad faces of the same 4 actors and 4 actresses
including 6 Caucasoid, 1 Negroid, and 1 Mongoloid from the NimStim
21
collection
that have high validity and reliability of expressions. Three masks (presented for 0.3 s
each) and two emotional faces (displayed for 0.020 s, 0.027 s, 0.033 s, 0.040 s or
0.047 s) were presented alternately on a screen (see Figure 1a). To maximise the
effects in the main learning task, we did not use fearful or neutral faces in this task. We
reasoned that prior knowledge of the facial expressions might affect
participant’s behaviour in the main learning task. Additionally, repetitive
presentation of the same emotional pictures could lead to reduced stimulus saliency.
Participants were required to discriminate the two expressions of an identical actor
or actress by answering whether the first expression was the ‘‘same’’ as the second one
within 3.0 s. Participants indicated their answers by pressing a button with the
right index (same) or ring (different) fingers. Additionally, they were asked to indicate
how confident they were in their answers (‘‘low confidence’’, ‘‘medium confidence’’,
or ‘‘high confidence’’) with the right index, middle, and ring fingers, respectively.
As we used two different pictures of an identical actor or actress with forward and
backward masks for each trial, participants could not judge the difference of
expressions based on outlines of faces or afterimages. This task included 80 trials
(8 same and 8 different trials 35 presentation conditions in a pseudo-random order).
As the participants were trained for several practice trials with another stimulus set
(happy and sad faces), they executed this task flawlessly.
Learning task. For the main learning task, participants learned probabilistic
associations (65% or 35%) between four visual cues and two rewards (¥100 or ¥1)
through trial and error (Figure 2a). The design was similar to a previous experimental
paradigm
3
except for the brief presentation of facial expressions. Each participant was
randomly assigned to one of four face-presentation durations (0.027 s, 0.033 s,
0.040 s, or 0.047 s). We used a between-participants design for the four durations
because of task difficulty and to avoid the effects of repetition, such as habituation to
the task or meta-learning of task structure
22
.
Face stimuli were 20 fearful and 20 neutral faces of 10 actors and 10 actresses,
including 10 Caucasoid, 7 Negroid, and 3 Mongoloid. Just before the visual cue
(0.3 s), either a fearful or neutral face interleaved with four masks (0.3 s) was
presented three times on a screen for an individually and randomly assigned duration
in a pseudo-random order. Only one emotion was used within a given trial.
Following the last face, one of the cues was presented, followed by a choice between
¥100 and ¥1. Participants then pressed a button within 1.5 s to indicate which of the
two rewards they expected. The order of cue presentation and the assignment of
the two buttons (left or right) with rewards were randomised across trials. After
making their ch oice, the actual reward was shown in yellow letters for 1.0 s. Over
time, participants could then learn the association between each cue and the
corresponding reward. Before the experiments, we confirmed that the participants
fully understood this task. They were instructed that the face and noise presentations
would signal the appearance of a cue. No participants reported noticing any
associations between particular facial expressions and the cues. The combinations of
the four visual cues, facial expressions, and rewards were counterbalanced across
participants (Figure 2b). The total number of trials was 320 (80 3 4 conditions).
Statistical analyses for perceptive discrimination task. The correct rates (CR) were
calculated by dividing the sum of the hit rate and correct rejection rate by the number
of trials (16) (Figure 1b red). We calculated the subjective confidence level for
each judgment using the confidence score index (CSI). For this index, each raw rating
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SCIENTIFIC REPORTS | 5 : 8478 | DOI: 10.1038/srep08478 5
was 1, 2, or 3, representing ‘‘low confidence’’, ‘‘medium confidence’’, or ‘‘high
confidence’’, respectively. This rating was independent of the correctness of the
judgment, and was averaged for each duration (1 # CSI # 3) (Figure 1b black).
Additionally, we sorted the CSI data based on the CR (Supplementary Fig. S1).
Statistical analyses for sampling bias . The learning task was conducted using a
between-participants design for the four presentation durations to avoid fatigue,
habituation, and meta-learning of task structure
22
. However, this might have induced
sampling bias. We therefore examined four possible biases: age, sex, the time of day
the experiment started, and the intelligence level based on university-department
academic scores. The mean experimental start time was taken into account because
experiments conducted in the early morning or late at night may be associated with
different arousal levels, even though we reminded participants by email before
participation to get enough sleep. Results are summarised in Table 1 and there was no
bias in any of the four groups.
Reinforcement learning model-based analysis. To conduct a trial-based analysis of
the learning process, we adopted a reinforcement learning model
3,23,24
. This model
assumes that each participant assigns the value function Q
t
(s
t
, a
t
) to action a
t
for the
cue s
t
at time t. Learning increases the accuracy of value representation by updating
the value in proportion to the reward prediction error (RPE) R
t
2 Q
t
(s
t
, a
t
), which is
the difference between the expected and actual reward at time t (Equation 1):
Q
tz1
s
t
,a
t
ðÞ~Q
t
s
t
,a
t
ðÞze
f
R
t
{Q
t
s
t
,a
t
ðÞðÞ: ð1Þ
Our learning model contains four free parameters: a learning rate (e
f
), reward
sensitivity (d
f
), value-independent bias for the choice of ¥100 (a
t
), (b
f
(a
t
)), and an
exploration parameter (b
f
). The learning rate controls the effects of the RPE, and
reward sensitivity transforms the actual reward (r
t
) in yen into a subjective reward
(R
t
) for each participant (Equation 2):
R
t
~d
f
r
t
: ð2Þ
In relation to behavioural choice (Equation 3), the bias term represents a value-
independent bias or inclination towards the choice of ¥100, and the exploration
parameter controls how deterministically the value function leads to an advantageous
behaviour:
Pa
t
js
t
ðÞ
~
exp b
f
Q
t
s
t
,a
t
ðÞzb
f
a
t
ðÞ
P
a’
exp b
f
Q
t
s
t
,a
t
ðÞzb
f
a’
t
ðÞ
: ð3Þ
We estimated each participant’s free parameters (denoted as the vector h) from their
trial-by-trial learning using the maximum likelihood-estimation method, which
minimises the negative log-likelihood of the participant’s behaviour (D), as shown in
equations 4 and 5. This non-linear minimisation of equation 4 was conducted using
the MATLAB function ‘‘fmincon’’.
min{log PDjhðÞ ð4Þ
PDjhðÞ~ P
t
Pa
t
js
t
ðÞ ð5Þ
The probability of choosing an action, a
t
(¥100 or ¥1), given a visual cue, s
t
,was
computed based on equation 3.
We evaluated the significance of each parameter using Akaike information criteria
(AIC) and Bayesian information criteria (BIC) by comparing four models using the
learning rate and exploration parameter (eb), eb with reward sensitivity (ebd), eb with
¥100 bias (ebb), and eb with both reward sensitivity and ¥100 bias (ebdb). We
calculated these information criteria for each participant and compared the mean
scores (n 5 91).
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Author contributions
N.W. and M.H. designed the experiments. N.W. performed the experiments. N.W. and
M.H. analysed the data, and wrote and reviewed the manuscript.
Additional information
Supplementary information accompanies this paper at http://www.nature.com/
scientificreports
Competing financial interests: The authors declare no competing financial interests.
How to cite this article: Watanabe, N. & Haruno, M. Effects of subconscious and conscious
emotions on human cue–reward association learning. Sci. Rep. 5, 8478; DOI:10.1038/
srep08478 (2015).
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