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Cortical responses to dynamic emotional facialexpressions generalize across stimuli, and aresensitive to task-relevance, in adults with andwithout Autism
Dorit Kliemann a,*, Hilary Richardson b, Stefano Anzellotti b,Dima Ayyash b, Amanda J. Haskins b, John D.E. Gabrieli a andRebecca R. Saxe b
a McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, MA, USAb Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA
a r t i c l e i n f o
Article history:
Received 9 September 2017
Reviewed 29 October 2017
Revised 11 January 2018
Accepted 8 February 2018
Action editor Holger Wiese
Published online 21 February 2018
Keywords:
Social cognition
fMRI
Emotional faces
MVPA
Autism
* Corresponding author. McGovern InstituteCambridge, MA 02139, USA.
right middle superior temporal sulcus; ROI, region of
interest; lpSTC, left posterior superior temporal cortex.
Table 5 e Bayes Factor [odds by which the null hypothesis(no group difference) is favored] for the social brain ROIscombined (all) and per study (Study 1, Study 2).
ROI All Study 1 Study 2
DMPFC 21.7 13.1 14.9
MMPFC 6.7 3.6 12.7
rFFA 11.6 11.5 11.2
rmSTS 20.1 9.7 10.8
lpSTC 7.8 8.8 8.6
Abbreviations: ROI, region of interest; DMPFC, dorso-medial pre-
frontal cortex; MMPFC,middle-medial prefrontal cortex; rFFA, right
fusiform gyrus; right middle superior temporal sulcus; lpSTC, left
posterior superios temporal cortex.
c o r t e x 1 0 3 ( 2 0 1 8 ) 2 4e4 3 35
3.3.2.3. COMBINING STUDY 1 AND STUDY 23.3.2.3.1. ROI BASED MVPA ANALYSES. Study 1 and Study 2
both tested perception of valence in brief dynamic facial ex-
pressions, using slightly different stimuli and tasks. We
combined data from these studies into one large sample to
increase power to detect potential group differences.
We first tested for overall classification of valence. Over all
participants, we found significant classification accuracies in
all social brain ROIs [DMPFC, mean ¼ 54.99 (SD ¼ 8.03),
t(79) ¼ 5.56, p ¼ 3.5 � 10�7; MMPFC, mean ¼ 53.64 (SD ¼ 8.02),
t(79) ¼ 4.06, p ¼ 1.2 � 10�4; rFFA, mean ¼ 53.36 (SD ¼ 8.00),
t(79) ¼ 3.76, p ¼ 3.3 � 10�4; rmSTS, mean ¼ 54.13 (SD ¼ 8.37),
t(79) ¼ 4.42, p ¼ 3 � 10�5; lpSTC, mean ¼ 53.21 (SD ¼ 8.64),
t(79) ¼ 3.32, p ¼ .001].
A repeated measures ANOVA testing directly for group
differences again revealed no significant main effect of group
[F(1,76) ¼ .077, p ¼ .782, hp2 ¼ .001] or interaction of group by
ROI [F(1,76) ¼ .1.31, p ¼ .265, hp2 ¼ .017].
To test the effect of group on valence classification in all
collected data across studies, and to test for interactions of
group with other potentially relevant factors (i.e., sex, hand-
edness, IQ, motion, study; see Section 2 for model specifica-
tion), we conducted a linear mixed effects regression analysis.
The results of this model again showed no significant main
effects or interactions with group (all p > .5 see Table 4 for
details on the model statistics).
Weighing the evidence for and against a group difference
between the ASD and NT group with a Bayes analysis
approach resulted in moderate evidence in favor of the null
hypothesis for all five ROIs tested for each study separately,
and stronger evidence when combining all data (see Fig. 4
plotting the weights and Table 5). Using all data from both
studies (n¼ 89) the odds in favor of the null hypothesis in each
ROI range between 6:1 (MMPFC) and 21:1 (DMPFC). Thus, the
current results suggest reasonable confidence in accepting the
null hypothesis that there are no group differences in valence
extraction from the social brain regions tested.
In sum, these analyses suggest that the valence of dynamic
facial expressions is represented in response patterns of social
brain regions, in both adults diagnosed with ASD and typically
developing control participants. Although supporting the null
hypothesis with regards to group differences, these are not
“null results”: on the contrary, significantly above-chance
classification of valence was obtained across ROIs for both
groups.
Univariate analyses similarly revealed no group difference
in average magnitude of response in any region (see
Supplementary material for details).
3.3.2.3.2. WHOLE BRAIN SEARCHLIGHT-BASED MVPA. To test
whether group differences might exist outside our a priori
ROIs we conducted a searchlight procedure across the whole
brain in the combined data from Study 1 and Study 2. Across
all participants, the whole brain searchlight revealed five
significant clusters where patterns of activity could classify
valence (p< .05, k> 9, FWE correction for multiple compari-
son): dorsal medial prefrontal cortex, superior and middle
temporal gyrus, left postcentral gyrus and middle occipital
gyrus (see Table 6 and Fig. 5). However, no clusters showed
differential classification across groups (NT > ASD, or
NT > ASD).
3.3.3. Generalization of valence information across stimulusformats (Study 1)Abstract information about a character's emotional valence
would generalize across different formats of stimulus (facial
expressions and animated situations). We trained a valence
classifier on patterns of activity in one stimulus condition
(e.g., expressions) and tested the classification accuracy in the
other stimulus condition (e.g., situations). As reported in
Skerry and Saxe (2014), in control participants, classification
of valence when generalizing across stimulus type was
Table 7 e Test for inequality of variances in classificationaccuracies for encoding valence from facial expressions.
ROI Study F(df) p
DMPFC Study 1 .001 (35) .973
Study 2 .022 (50) .882
Combined .004 (78) .952
MMPFC Study 1 .758 (35) .390
Study 2 .144 (50) .705
Combined 1.473 (78) .29
rFFA Study 1 .144 (50) .705
Study 2 2.23 (35) .144
Combined .014 (78) .907
rmSTS Study 1 .519 (35) .476
Study 2 .002 (50) .967
Combined .140 (78) .710
lpSTC Study 1 .352 (35) .557
Study 2 3.983 .051
Combined 2.707 .104
Statistics of the Levene test. Abbreviations: F, F-statistic; df, degrees
of freedom; p, Significance value.
Table 8 e Test for inequality of variances in classificationaccuracies for valence independent from stimulus-type(Study1, faces vs situations) and during age attribution(Study 2).
ROI Valenceindependent ofstimulus-type
(Study1)
Valence duringage attribution
(Study 2)
F(df) p F(df) p
DMPFC .023 (35) .881 1.391 (50) .244
MMPFC .671 (35) .418 1.605 (50) .211
rFFA 1.317 (35) .259 .314 (50) .578
rmSTS .277 (35) .602 2.106 (50) .153
lpSTC .476 (35) .495 .579 (50) .450
Statistics of the Levene test. Abbreviations: F, F-statistic; df, degrees
of freedom; p, Significance value.
c o r t e x 1 0 3 ( 2 0 1 8 ) 2 4e4 3 39
Morey, & Iverson, 2009) (Fig. 4, Table 3). There was also no
greater variability in neural measures for the ASD group.
Theoretically, the absence of robust group differences is
important because the experiment was a sensitive test of a
widespread assumption about the mechanism of social
impairment in ASD in general, while addressing valence pro-
cessing prototypically (Ben Shalom et al., 2006; Celani,
Battacchi, & Arcidiacono, 1999; Kuusikko et al., 2009; Tseng
et al., 2014). First, all of the stimuli were dynamic videos,
and covered basic as well as more complex/social emotions
(e.g., angry, surprised, enthusiastic, furious), wide ranges of
expressivity (frommore subtle to overstated expressions), and
a diverse set of individuals (Study 1: 96 characters, Study 2: 20
characters), spanning a wide age range and both genders.
Stimuli in Study 1 were subtle and less controlled (with
respect to lighting and viewpoint), hence reflecting more
naturalistic perceptual content. Stimuli in Study 2 were
exaggerated and more controlled (i.e., all with overhead
lighting and frontal view). Yet for both sets of stimuli, brain
responses to emotional valence were not different in in-
dividuals with or without ASD.
Second, the multivariate measure of brain region re-
sponses used here is more sensitive than traditional univari-
ate measures (although note that we observed no group
difference in average magnitude of response in any region
either, see Supplementary material for details). Multivariate
We thank Amy Skerry for design and data collection in Study 1
and Ralph Adolphs for comments on earlier versions of this
manuscript. D.K. was in part supported by a Feodor-Lynen
Postdoctoral Fellowship of the Alexander von Humboldt so-
ciety. This work was supported by the NIH grant 4-R01-
MH096914-05 and by a grant (project number 6925173) from
the Simons Foundation to the Simons Center for the Social
Brain at MIT.
Supplementary data
Supplementary data related to this article can be found at
https://doi.org/10.1016/j.cortex.2018.02.006.
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