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  <front>
    <journal-meta />
    <article-meta>
      <title-group>
        <article-title>The Capacity For Implicit Social Learning In Relation To Autistic Traits</article-title>
      </title-group>
      <contrib-group>
        <contrib contrib-type="author">
          <string-name>Dr Tjeerd Jellema (T.Jellema@hull.ac.uk)</string-name>
          <xref ref-type="aff" rid="aff0">0</xref>
          <xref ref-type="aff" rid="aff1">1</xref>
        </contrib>
        <aff id="aff0">
          <label>0</label>
          <institution>Department of Psychology, University of Hull HU6 7RX</institution>
          ,
          <country country="UK">United Kingdom</country>
        </aff>
        <aff id="aff1">
          <label>1</label>
          <institution>Sylwia Macinska</institution>
        </aff>
      </contrib-group>
      <fpage>554</fpage>
      <lpage>559</lpage>
      <abstract>
        <p>People learn social cue-outcome relationships and use this knowledge to guide their behavior, even in the absence of explicit knowledge of social contingencies. The aim of the current study was to investigate variations in implicit social learning abilities between typically developed individuals with low and high number of autistic traits, as assessed by the AQ questionnaire. In the learning phase, participants repeatedly observed two different identities whose gaze direction and facial expression were manipulated to convey either a pro- or anti-social disposition toward the observer. These dispositions were determined by specific contingencies between these cues. Crucially, the participants were not aware of these contingencies (as confirmed in the debrief session). In the test phase, the participants showed specific biases in their perceptual report of morphs of the two identities, which reflected that they had implicitly learned the identities' dispositions. The results indicated that in the current paradigm others' dispositions can be learned implicitly (i.e. without awareness of the cue contingencies), and that this ability is correlated with AQ scores; participants with higher AQ scores showed less implicit social learning than those with lower AQ scores.</p>
      </abstract>
      <kwd-group>
        <kwd>Implicit learning</kwd>
        <kwd>Autism spectrum disorder</kwd>
        <kwd>Intuition</kwd>
        <kwd>Social cognition</kwd>
        <kwd>Emotional facial expression</kwd>
      </kwd-group>
    </article-meta>
  </front>
  <body>
    <sec id="sec-1">
      <title>Introduction</title>
      <p>People exchange large numbers of nonverbal cues, which
are typically interpreted in a seemingly effortless manner.
The ability to encode and decode social information is
crucial to successfully navigate the social world. This social
competence seems to be employed automatically and
involuntarily; people have a tendency to attribute
dispositional causes to non-verbal behavior in order to
obtain a quick impression of other’s thoughts and feelings,
rather than using effortful cognitive processes and deliberate
reasoning.</p>
      <p>
        Implicit (social) learning is widely assumed to play a
central role in social cognition and is regarded as a cognitive
substrate of social intuition (Lieberman, 2000). According
to Lieberman, social intuition involves making rapid
judgments about the emotions, intentions or attitudes of
others on the basis of learned sequences of nonverbal cues,
such as subtle facial expressions and bodily gestures. People
learn social cue-outcome relationships and use this
knowledge to guide their behavior, even in the absence of
explicit knowledge of social contingencies (Lewicki, Hill,
Czyzewska, 1992). Social cues may implicitly acquire value
on a short timescale, sometimes within the space of a single
interaction
        <xref ref-type="bibr" rid="ref6">(Heerey &amp; Velani, 2010)</xref>
        .
      </p>
      <p>
        Given the importance of social intuition, an impaired
ability to implicitly encode and decode social cues might
result in difficulty adjusting behavior to the demands of
social situations. Indeed, such an impairment has been
proposed to be a crucial factor underlying the social
deficiencies in autism spectrum disorders
        <xref ref-type="bibr" rid="ref5">(ASD; Frith &amp;
Frith, 1999)</xref>
        . ASD is characterized by deficits in social
interaction and social communication, including nonverbal
communicative behaviors. As a result, individuals with
ASD are likely to misinterpret social cues and engage in
socially inappropriate behavior. It has been argued that the
social impairments in ASD are linked to an impaired theory
of mind; the ability to understand others as intentional
agents, that is, to interpret their minds in terms of intentional
states such as desires and beliefs
        <xref ref-type="bibr" rid="ref1">(Baron-Cohen, 2000)</xref>
        .
There are indications that social deficits seen in individuals
with ASD are especially related to failure in automation of
social cue processing rather than in the ability to understand
intentions per se
        <xref ref-type="bibr" rid="ref8">(Jellema et al., 2009; Senju, Southgate,
White &amp; Frith, 2009)</xref>
        . This may be compensated for through
deliberate reasoning about others’ intentions. However, the
interpretation of social cues using effortful cognitive
processes would be much slower and possibly less accurate
than in involuntary processing.
      </p>
      <p>
        Nevertheless, a recent meta-analysis looking at implicit
learning in individuals with ASD did not find any anomalies
on a number of implicit learning tasks
        <xref ref-type="bibr" rid="ref4">(Foti et al., 2014)</xref>
        .
However, the reported studies examined implicit learning in
non-social domains, with tasks such as artificial grammar
learning, serial reaction task or contextual cueing. There is
an emerging body of research suggesting that implicit
learning is not a global impairment, but rather may be found
either intact or impaired depending on the type of the
information to be learned
        <xref ref-type="bibr" rid="ref10">(Travers et al., 2013)</xref>
        .
      </p>
      <p>
        The autism spectrum condition could be considered as a
scale of social aptitude with autistic traits found throughout
the population to differing degrees, with clinical levels of
autism at the high end of this continuum
        <xref ref-type="bibr" rid="ref3">(Constantino &amp;
Todd, 2003)</xref>
        . The Autistic-spectrum Quotient (AQ)
questionnaire is one of the measures that has been
developed to gauge autistic traits in the population at large
        <xref ref-type="bibr" rid="ref2">(Baron-Cohen et al., 2001)</xref>
        . It is a self-report questionnaire
with a maximum score of 50, where a score of 32 or higher
may meet the diagnostic criteria for ASD
        <xref ref-type="bibr" rid="ref2">(Baron-Cohen et
al., 2001)</xref>
        . Although not currently used as a diagnostic tool,
the questionnaire has been found to be a sustainable
indicator of ASD with 83% of accuracy (Woodbury-Smith,
Robinson, Wheelwright, &amp; Baron-Cohen, 2005). As
typically developed individuals with relatively high levels
of autistic traits are likely to share some social and cognitive
deficits with individuals with ASD, it should be possible to
test typically developed individuals with varying AQ scores
to enhance our understanding of ASD
        <xref ref-type="bibr" rid="ref7">(Hudson, Nijboer, &amp;
Jellema, 2012)</xref>
        .
      </p>
    </sec>
    <sec id="sec-2">
      <title>Current Study</title>
      <p>The aim of the current study was to investigate whether
implicit social learning would take place in a simple
computer-based task, and whether there are variations in
implicit social learning abilities in typically developed
individuals that vary in autistic traits (AQ). It was
hypothesized that higher AQ scores would be correlated
with poorer implicit social learning. In the current study,
two types of nonverbal social cues were manipulated to
affect social judgments: emotional expression and gaze
direction. Participants were hypothesized to implicitly learn
the agent’s disposition toward them on the basis of specific
combinations of these two cues. The experiment consisted
of an initial learning phase, followed by a test phase, in
which the extent of learning was measured.</p>
    </sec>
    <sec id="sec-3">
      <title>Methods</title>
    </sec>
    <sec id="sec-4">
      <title>Participants</title>
      <p>Fifty-one undergraduate students (20 women) from the
University of Hull participated in the experiment in
exchange for course credit. All participants provided written
informed consent prior to the experiment. After exclusion of
one participant (see below) the mean age of participants was
21.3 (SD=2.77).</p>
    </sec>
    <sec id="sec-5">
      <title>Stimuli</title>
      <p>Stimuli were created using Poser 7 animation software
(Curious Labs, Inc., Santa Cruz, CA, &amp; e frontier, Inc.,
Scotts Valley, CA). Two male identities were used named
James and Simon. The characters were oriented facing the
observer throughout the presentation and were depicted
from the top of the shoulders upwards. The stimuli were
presented on a 21 inch monitor (100 Hz refresh rate) using
e-Prime software (Psychology Software Tools, Inc.,</p>
      <p>Sharpsburg, PA), at a distance of approximately 50cm from
the participant.</p>
    </sec>
    <sec id="sec-6">
      <title>Procedure</title>
      <p>
        Learning Phase The learning phase used in the current
study was broadly consistent with the learning phase of the
experiment conducted by
        <xref ref-type="bibr" rid="ref7">Hudson et al. (2012)</xref>
        . Participants
viewed 64 clips of two different identities, 32 for each
identity. Each clip consisted of 20 frames, the first and last
frame were displayed for 750 ms and the other 18 frames for
30 ms each. Two facial features were manipulated: gaze
direction and facial expression. Each clip started with the
gaze either directed towards the participant (direct gaze
direction) and then gradually averted horizontally until at a
30º angle away from the observer at the end of the clip
(indirect gaze direction), or began with a 30º aversion and
ended with direct gaze direction (the clip played
backwards). To manipulate facial expressions, the clip
began either with an identity displaying a happy expression,
which gradually morphed into an angry expression, or began
with an angry expression which morphed into a happy
expression (clip played backwards).
      </p>
      <p>Crucially, each identity portrayed a different combination
of gaze direction and emotional expression, such that each
could be said to have a different disposition toward the
observer (Figure 1). For identity A, gaze averting away from
the observer was accompanied by a change from a happy to
an angry expression, while gaze movement towards the
observer was accompanied by a change from angry to happy
(played backward). This identity can therefore be inferred to
hold a pro-social disposition toward the observer; smiling
when looking at the person and frowning when looking
away. For identity B, the reverse cue combinations were
used and this identity can therefore be inferred to hold an
antisocial disposition toward the observer.</p>
      <p>Each identity displayed happy and angry expressions for
exactly the same amount of time and looked at and away
from the observer for exactly the same amount of time. This
was to ensure that a social disposition could only be learnt
on the basis of the specific combination of two cues; each
cue on itself could not cause any social learning effects. The
social disposition of the character used in the study was
counterbalanced across participants; for half of the
participants James was holding a pro-social disposition
while Simon was holding an anti-social disposition
(Experiment 1), while for the other half Simon was the
prosocial and James the anti-social identity (Experiment 2).</p>
      <p>Debriefing Phase Directly following the learning phase,
participants were required to give verbal responses to a
series of questions checking whether they had picked up the
cue-identity contingencies. The questions were: (1) Could
you describe what you just have seen? (2) How many
different identities did you see? (3) What can you tell me
about their facial expressions? (4) What can you tell me
about their gaze direction? (5) Did you detect certain
patterns between facial expressions, gaze directions and
identities? Answers were manually recorded.</p>
      <p>Testing Phase In the testing phase, a morph of the two
identities was presented in the centre of the screen, with the
faces of James and Simon displaying neutral expressions on
either side of the morphed identity (Figure 2). The morphed
identity was either smiling or frowning, and was composed
of different proportions of either, the smiling James and the
smiling Simon or the frowning James and the frowning
Simon. Five morph levels (proportions) were used: M1 =
60% pro-social and 40% anti-social, M2 = 55% pro-social
and 45% anti-social, M3 = 50% pro-social and 50%
antisocial, M4 = 45% pro-social and 55% anti-social, M5 =
40% pro-social and 60% anti-social. There were in total 20
test trials (5 morph levels x 2 emotions x 2 repetitions).
Participants were required to select whether the morphed
identity resembled more closely the pro-social identity (key
1) or the anti-social identity (key 2) The rationale was that
when participants would have implicitly learned that
identity A had a pro-social disposition and identity B an
anti-social disposition toward them, then they would be
more likely to judge the smiling morph as more similar to
identity A, and the frowning morph as more similar to
identity B, because intuitively identity A would be
associated with a ‘positive’ and identity B with ‘negative’
attitude.</p>
      <p>AQ Questionnaire At the end of the experiment,
participants completed an online version of the AQ
(BaronCohen et al., 2001).</p>
    </sec>
    <sec id="sec-7">
      <title>Results</title>
      <p>The debriefing phase indicated that one participant had
discovered the cue-identity contingency and his data was
removed from the analysis.</p>
      <p>The dependent variable consisted of mean scores on the
five levels of morphs used in the test phase. A score of 1
indicated that participants believed the morph resembled the
pro-social identity more than the anti-social identity, while a
score of 2 indicated that participants believed the morph
resembled the anti-social identity more than the pro-social
one.</p>
      <p>Two separate experiments were conducted on two
participant groups, none of the participants participated in
both experiments. In Experiment 1, James had the pro-social
disposition and Simon the anti-social disposition; in
Experiment 2 the dispositions were reversed. The data from
both experiments was analyzed using a 2x5x2 repeated
measures ANOVA with Morph Facial Expression (happy,
angry) and Morph Level (M1, M2, M3, M4, M5) as
withinsubject factors and Experiment (Exp1, Exp2) as
betweensubjects factor.</p>
      <p>The main effect of the factor Morph Facial Expression
was significant (F1,48 = 6.7, p = .013, ηp2 = .12), with higher
scores for the angry morph than for the happy morph. This
indicated that implicit learning had taken place. The Morph
Facial Expression x Experiment interaction was
nonsignificant (F1,48 = .30, p = .59, ηp2 = .006). The main effect
of Morph Level was significant (F4,192 = 33.4, p &lt; .001, ηp2
= .41), indicating that participants were sensitive to the
different morph proportions. The main effect of Experiment
was non-significant (F1,48 = 3.28, p = .076, ηp2 = .064). The
remaining 2-way interactions, and the 3-way interaction,
were all non-significant (all p’s &gt; .16) (Figure 3, top panel).</p>
      <p>The mean AQ score was 15.5 (SD = 5.6), ranging from 5
to 32. A correlation analysis for the mean difference score
[mean score for Happy Morph across the 5 morph
proportions minus mean score for Angry Morph across the 5
morph proportions] and the individual AQ scores revealed a
significant negative correlation (r = -.287, p = .043),
reflecting that an increase in the level of autistic traits
corresponded with a decrease in the extent of implicit social
learning.</p>
    </sec>
    <sec id="sec-8">
      <title>Discussion</title>
      <p>The main finding was that in the current paradigm typically
developed individuals were capable of implicit social
learning. It suggests that the pro- or anti-social dispositions
of another individual can be implicitly understood on the
basis of specific social cue combinations conveyed in a
social encounter, without one being aware of the
contingencies. The implicitly learned dispositions may serve
as useful predictors of an individual’s future behaviour,
affecting one’s subsequent responses to that individual. A
second important finding was that this effect is influenced
by individual differences in autistic traits. Those with less
autistic traits (low AQ score) implicitly learned the social
dispositions better than those with more autistic traits (high
AQ score). Presumably, those with lower AQ scores are
better in ‘picking up’ the meaning of social contingencies.</p>
      <p>
        It is tempting to speculate about the implications of the
current findings for individuals with ASD. In line with the
theory of an autism spectrum continuum
        <xref ref-type="bibr" rid="ref2">(Baron-Cohen et
al. 2001)</xref>
        , extrapolation of the results of the high AQ group
to individuals with ASD would suggest more severe deficits
in the implicit social learning ability in ASD, which might
underpin core deficits in social understanding in ASD.
      </p>
      <p>According to a recent account, sensitivity to social signals
such as direct eye gaze is essential for learning through
social interaction (Sodian, Schuwerk &amp; Kristen, 2015).
Impaired processing of social cues in ASD could explain
insufficient learning from others and the same may be
expected of those with high AQ scores.</p>
      <p>
        However, it is not quite clear whether individuals with
high AQ scores are less receptive to social cues per se, or
whether they are equally receptive, but have a diminished
ability to learn associations between emotions and specific
individuals. Face identity processing has been found to be
impaired in people with ASD for tasks that require face
memory
        <xref ref-type="bibr" rid="ref11">(Weigelt, Koldewyn &amp; Kanwisher, 2012)</xref>
        . This
deficit is much stronger when a delay intervenes between
two presentations of an identity. However, in the current
study the morphs in the testing phase were presented
simultaneously with the faces of both identities, which
should have reduced memory demand for this particular
task.
      </p>
      <p>It is important to note that the task employed in this study
is a simple computer task, which is only a human-artefact
representation of a social interaction. While the
undercomplexity of the experimental design allows controlling
for extraneous/confounding variables, the results of the
current study need to be approached with caution when
generalising to naturalistic settings.</p>
      <p>There is also a possibility that the variations in implicit
learning between individuals low and high in autistic traits
may be due to low-level visual learning, rather than to a
form of social learning. The face configuration of a happy
morph involves eyes looking at the participant and a smiling
mouth, which is a closer visual match to the happy
prosocial face than the angry anti-social face, which has the
eyes averted. Similarly, the angry morph is a closer visual
match to the angry anti-social face. If the learning occurred
on the basis of the closer matching of low-level features –
eye and mouth configuration – it would indicate that
individuals high in autistic traits show deficits in implicit
learning that are not exclusive to the social domain.
Subsequent studies, involving non-social stimuli, will
investigate whether the lower propensity for implicit
learning in the high AQ group is specific to the social
domain and does not apply to non-social learning, or
whether it is a more generalised impairment.</p>
      <p>It is as yet unknown whether the deficits in implicit social
learning in the high AQ group are specific to implicit social
learning and does not apply to explicit social learning. The
lack of automatic processing of social cues may be
compensated for through deliberate reasoning about others’
intentions. For example, Senju and colleagues (2009) found
a striking dissociation between implicit and explicit theory
of mind; while the performance of individuals with ASD on
an implicit theory of mind task revealed intriguing
difference from that of controls, they showed intact explicit
theory of mind. As a result, one may expect intact explicit
social learning in individuals with high AQ scores.
However, the interpretation of social cues using effortful
cognitive processes would be much slower and possibly less
accurate than in involuntary processing, which may be the
primary reason for difficulties in social interactions found in
ASD. Future studies should contrast the ability for implicit
and explicit learning in relation to AQ scores.</p>
      <p>In summary, this study provided evidence that people are
capable of learning contingencies between social cues and
use this knowledge to guide their behavior, even in the
absence of explicit knowledge. Furthermore, this effect is
related to individual differences in autistic traits, with
individuals low in autistic traits outperforming individuals
high in autistic traits. If the present pattern of results would
be more profound in an ASD sample, then that might help to
explain their inefficiency in using social cue-outcome
relationships to modulate their behavior.</p>
      <p>SM and MK were funded by Hull University studentships.</p>
    </sec>
    <sec id="sec-9">
      <title>Acknowledgments References</title>
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