Impaired executive control of emotional information in social anhedonia

Article (PDF Available)inPsychiatry Research 197(1-2):29-35 · March 2012with29 Reads
DOI: 10.1016/j.psychres.2011.12.023 · Source: PubMed
Abstract
We examined the executive control of emotional information and its relationship to social functioning in individuals at risk for schizophrenia, defined by high social anhedonia (SA). Using the same structure as the Attentional Network Test (ANT), we developed a measure of executive control of emotional information (ANT-Emotion) in which subjects identify the direction of an arrow flanked by irrelevant angry or neutral faces. Subjects completed the ANT, ANT-Emotion, and the Social Adjustment Scale, Self-Report (SAS-SR), a measure of social functioning. While there were no group differences in the alerting, orienting, and executive control networks assessed by the ANT, high SA individuals exhibited a specific impairment in the executive control of emotional information. High SA individuals also reported poorer social functioning. However, executive control of emotional information did not mediate the relationship between SA and social functioning. These findings indicate that, in high-risk populations, the impaired ability to inhibit emotional information allows negative affective stimuli to exert inappropriate influence on cognitive processes. These results are consistent with studies indicating similar findings in schizophrenia patients, suggesting that impaired inhibition of negative emotion may be part of the liability for the disorder.
Impaired executive control of emotional information in social anhedonia
Laura M. Tully
, Sarah Hope Lincoln, Christine I. Hooker
Psychology Department, Harvard University, Massachusetts, USA
abstractarticle info
Article history:
Received 15 January 2011
Received in revised form 20 August 2011
Accepted 12 December 2011
Keywords:
Psychosis-proneness
Schizophrenia
Attention
Attention network test
Social cognition
Social functioning
We examined the executive control of emotional information and its relationship to social functioning in individuals
at risk for schizophrenia, dened by high social anhedonia (SA). Using the same structure as the Attentional Network
Test (ANT), we developed a measure of executive control of emotional information (ANT-Emotion) in which sub-
jects identify the direction of an arrow anke d by irrelevant angry or neutral faces. Subjects completed the ANT,
ANT-Emotion, and the Social Adjustment Scale, Self-Report (SAS-SR), a measure of social functioning. While there
were no group differences in the alerting, orienting, and executive control networks assessed by the ANT, high SA
individuals exhibited a specic impairment in the executive control of emotional information. High SA individuals
also reported poorer social functioning. However, executive control of emotional information did not mediate the
relationship between SA and social functioning. These ndings indicate that, in high-risk populations, the impaired
ability to inhibit emotional information allows negative affective stimuli to exert inappropriate inuence on cogni-
tive processes. These results are consistent with studies indicating similar ndings in schizophrenia patients, sug-
gesting that impaired inhibition of negative emotion may be part of the liability for the disorder.
© 2012 Elsevier Ireland Ltd. All rights reserved.
1. Introduction
Social anhedonia (SA), a lack of pleasure from social interactions
that is distinguishable from social anxiety (Brown et al., 2007), is
thought to be a core feature of schizophrenia that contributes to the
liability of developing the disorder, and a key factor underlying the
social difculties seen in the illness (Meehl, 1962). SA predicts social
functioning in individuals with schizophrenia (Blanchard et al., 1998)
and high-risk populations (Cohen et al., 2006), is associated with ele-
vated symptoms (Horan et al., 2007), and predicts conversion to
schizophrenia-spectrum disorders (Kwapil, 1998). Similar to schizo-
phrenia patients, socially anhedonic individuals also exhibit decits
in attention (Gooding et al., 2006b) and emotion processing
(Phillips and Seidman, 2008). In line with data demonstrating social
cognitive processes act as mediators between cognitive impairments
and functional outcome (Green et al., 2000) the present research ex-
amines attentional processes in relation to emotional information in
individuals high in social anhedonia. We hypothesize that attentional
decits affect social functioning via a specic domain of social cogni-
tion, the executive control of socially relevant emotional information,
and that this relationship is part of an underlying vulnerability ob-
servable in psychosis-prone populations.
1.1. Attention & the attention network test
Attentional decits in schizophrenia and psychosis-prone populations
are well documented (Heinrichs and Zakzanis, 1998; Nuechterlein et al.,
1998) but the mechanisms by which attentional processes inuence so-
cial functioning are unknown. To understand attentional mechanisms
and how they contribute to social impairments in SA a measure that
can dissociate between specic domains of attention is needed. A promis-
ing candidate is the Attention Network Test (ANT) (Fan et al., 2002), an
experimental measure of three proposed attention networks: alerting,
orienting and executive control (Posner and Petersen, 1990). The alert-
ing network manages the ability to achieve and maintain an alert
state, the orienting network manages the a bility to select and focus
on the to-be-attended stimulus, and the executive control network
manages the ability to resolve conict among responses and conse-
quently the regulation of cognitions and emotions (Posner et al.,
2002).
There is increasing evidence for a specicdecit in the executive
control network, as measured by the ANT, in schizophrenia (Wang
et al., 2005; Gooding et al., 2006a; Urbanek et al., 2009). However, it
is unclear whether this decit is a consequence of schizophrenia, or
if it is part of the liability for the disorder. Although executive control
has been examined using the ANT in positive schizotypy (Wan et al.,
2006), and individuals high in physical anhedonia (Dubal et al.,
2000), to our knowledge ANT performance has yet to be examined
in SA. Moreover, little is known about the contribution of decits in
the executive control network to social impairments in SA as execu-
tive control mechanisms have not yet been directly tied to social cog-
nition and functioning decits. We sought to examine 1) whether
Psychiatry Research 197 (2012) 2935
Corresponding authorat: Psychology Department, Harvard University, 33 Kirkland St.,
William James Hall 806, Cambridge, MA 02138, USA. Tel.: +1 857 207 5509.
E-mail address: ltully@fas.harvard.edu (L.M. Tully).
0165-1781/$ see front matter © 2012 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.psychres.2011.12.023
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executive control decits are present in high SA individuals, and
2) the role of the executive control network in a specic social cognitive
process, the executive control of emotional information.
1.2. Executive control of emotional information
Executive control of emotional information operationalized here
as the ability to control the extent that emotion inuences cognition
is critical for successful decision making and social interactions; if an
individual is unable to inhibit irrelevant emotional information in the
social array this could adversely affect social interactions. In schizophre-
nia, neuroimaging studies show dysfunctional activity in the lateral pre-
frontal corte x (Barch, 2005), a region involved in the regulation of
emotiononbehavior(Ochsner and Gross, 2005). In behavioral studies,
individuals with schizophrenia show increased latencies on the Stroop
task for threat-related or paranoid words compared to depressed indi-
viduals and healthy controls (Bentall and Kaney, 1989), and are more
inuenced by negative affective primes when rating the trustworthiness
of neutral faces (Hooker et al., 2011). Collectively, these ndings are in-
dicative of decits in the executive control of emotional information in
schizophrenia, and that these decits directly affect social behavior, po-
tentially contributing to social impairments. Thus, we were interested in
investigating whether psychosis-prone individuals also exhibit impair-
ments in the executive control of emotional information, and whether
these impairments relate to social functioning.
High SA is associated with executive functioning impairments (Tallent
and Gooding, 1999) and aberrant processing of affective information
(Kerns and Berenbaum, 2000), indicating that dysregulation of inhibitory
mechanisms, such as executive control, and emotion processing is present
premorbidly. However, the interplay between affective information and
executive control in SA has received limited attention in the literature. If
high SA is related to difculties in controlling the inuence of emotional
information on behavior, it may contribute to social deci ts. Thus, we
were interested in whether executive control of emotional information
is impaired in socially anhedonic individuals, and whether this mediates
the relationship between SA and social functioning.
1.3. The present research
The present research examined attentional processes, specically
the executive control of emotional information, and social functioning
in high SA individuals and healthy controls. We developed a direct mea-
sure based on the ANT: the ANT-Emotion, a anker task with orienting
cues in which participants identify the direction of an arrow anked by
irrelevant neutral or angry faces. SA was assessed with the Revised So-
cial Anhedonia Scale (Eckblad et al., 1982). We also administered the
ANT as a measure of pure attentional processes, and the Social Adjust-
ment ScaleSelf Report (Weissman et al., 1978)asameasureofsocial
functioning.
We directly tested the following predictions: 1) Compared to con-
trols, high SA individuals will exhibit attentional decits on both the
ANT, specically in executive control, and the ANT-Emotion, specically
in the executive control of emotional information. 2) High SA individuals
will report poorer social functioning compared to controls. 3) Executive
control of emotional information will mediate the relationship between
SA and social functioning.
2. Methods
2.1. Participants
34 high SA and 29 control partic ipants were recrui ted from the Greater Boston
Area. Participants were recruited as part of a larger stud y (N = 108) investigating
the relationship between psychosis-proneness, social cognition, and social func-
tioning in which they were screened for SA with the Revised Social Anhedonia
Scale (RSAS) (Eckblad et al., 1982), and also completed the Schizotypal Personality
Questionnaire (SPQ) (Raine, 1991). Candidate high SA participants were selected
from the larger study sample using the cut-off of 1.96 standard deviations above
the mean for their gender from no rmative data re ported by Kwapil (1998):scores
of 16 and above for females; 20 and above for males. In order to compare high SA
individuals to indiv iduals who are not at risk for sch izophren ia, candidate control
participants were individuals who scored below 1.96 standard devia tions from the
mean on the RSAS and within the 10% cutoffs of the SPQ from the normative data
reported by Raine (1991) (SPQ scores less than 8 or greater than 42). Thus, con-
trol participants were individuals with no elevated risk for schizophrenia, scoring
within the normal range of the SPQ and the RSAS. Excl usion criteria were: E nglis h
as a second language, IQ below 70, history of head trauma, neurological illness,
current or past axis I disorders, and active subst ance abuse wi thin the past six
months.
Demographic information and group differences are presented in Table 1. The
study was approved by the ethical review board at Harvard University. After study pro-
cedures were explained, participants gave written informed consent.
2.2. Materials & assessments
2.2.1. Social anhedonia
The Revised Social Anhedonia Scale (RSAS) (Eckblad et al., 1982)isa40item
true/false self-report scale comprising of questions measuring individuals de-
creased pleasure from social interactions. Exampleitemsinclude:Iattachvery
little importance to having close friends (keyed tru e) and Just being with friends
canmakemefeelreallygood (keye d false).
2.2.2. Psychiatric illness
Axis I disorders were assessed using the Structured Clinical Interview for DSM-IV
Axis I Disorders (First et al., 2002); clinical interviews were conducted by trained mas-
ter's level doctoral students and supervised by a licensed clinical psychologist (CH).
Reliability assessments conducted by an independent clinician on a random sample
of ten clinical interviews revealed a kappa of 0.67, indicating substantial diagnostic
agreement (Landis and Koch, 1977).
2.2.3. Intelligence
Full scale IQ scores were estimated using the vocabulary and matrix reasoning subtests
of the Weschler Abbreviated Intelligence Scale (WASI) (Wechsler, 1999).
2.2.4. Social functioning
Social functioning was assessed with the Social Adjustment Scale Self Report (SAS-SR)
(Weissman et al., 1978). The SAS-SR consists of 54 questions assessing six areas of function-
ing: work, social and leisure activities, relationships with extended family, role as marital
partner, parental role, and role within the family unit. Each area is rated across four catego-
ries of assessment: performance at expected tasks, level of conict with people, interper-
sonal relations, and feelings and satisfactions. Area scores are averaged together to create
one composite score of social functioning.
2.3. Tasks and stimuli
2.3.1. The ANT
The ANT (Fan et al., 2002) assesses the efciency of the orienting, alerting, and execu-
tive control attentional networks by measuring differences in reaction times to indicate the
direction of a central arrow across cue and anker conditions. Participants identify the di-
rection (left, right) of a target arrow that appears above or below a central xation cross.
The arrow is preceded by an asterisk cue that either alerts or orients participants to the up-
coming target. There are four cue types: no cue (neither alerting nor orienting), central cue
(on the xation cross; alerting), double cue (two asterisks presented simultaneously above
and below
xation; alerting), or spatial cue (a single asterisk above or below xation in the
location of the upcoming target; orienting). Immediately after the asterisk cue, the target
arrow appears and is anked by one of three anker types: congruent (arrows in the
same direction as the target arrow), incongruent (arrows in the opposite direction as the
target arrow) and neutral (horizontal lines). The alerting and orienting networks are
assessed via the different cue conditions, the executive control network is assessed via
the different anker conditions. Measures of the efciency of the three attentional networks
are obtained via simple subtractions of reaction times between conditions: alerting scores
are calculated by subtracting reaction times in the double cue condition from reaction
times in the no cue condition; orienting scores are calculated by subtracting reaction
times in the spatial cue condition from reaction times in the center cue condition; executive
control scores are calculated by subtracting reaction times in the congruent anker condi-
tion from reaction times in the incongruent anker condition.
The task consists of 288 trials; 72 in each of the four cue conditions. Each trial is 4000 ms
beginning with a xation cross, followed by one of the four cue types presented for 100 ms,
followed by an average interval of 400 ms after which one of the three target stimuli is pre-
sented for 1700 ms or until the subject responds (congruent, incongruent, neutral). The task
was presented on an IBM ThinkPad laptop using e-prime professional version 2.0.
2.3.2. The ANT-Emotion
Using the same structure as the ANT, the ANT-Emotion is designed to asse ss
the orienting an d executive control attentiona l networks in r elation to emotional
information. Orienting to emotional information is assessed by using faces (neutral, angry)
as spatial cues for the upcoming target. Executive control of emotional information is
assessed by using faces (neutral, angry) as ankers of the central target arrow. Participants
30 L.M. Tully et al. / Psychiatry Research 197 (2012) 2935
indicate the direction of a central arrow anked by one of three anker types: irrelevant
angry faces, irrelevant neutral faces, or neutral lines. The anker conditions are preceded
by one of three cue types (asterisk, neutral face, angry face) presented in one of two cue po-
sitions (central, spatial asinglecueaboveorbelowxation orienting participants to the
location of the upcoming target). Face cues never precede face ankers: in face anker con-
ditions the cue presented is always an asterisk; in neutral line anker conditions the cue
presented is either an angry or neutral face (see Fig. 1a and b for task illustration).
Measures of the efciency of each network are obtained through simple subtractions
of reaction times between conditions. Executive control of emotional information scores
are calculated by subtracting reaction times in the neutral face anker condition from re-
action times in the angry face anker condition. Orienting to emotional information scores
are calculated by subtracting reaction times in the neutral face spatial cue condition from
the angry face spatial cue condition. Orienting to emotional information was included in
the task in order to dissociate the attentional capture of emotional information from the
executive control of emotional information. If negative emotional faces are simply more sa-
lient for high SA participants we would expect faster orienting to emotional information
compared to controls; if, as predicted, high SA participants have difculty inhibiting nega-
tive emotional faces we would expect impaired executive control of emotional information.
The face stimuli are colored photographs of unfamiliar male and female faces taken from
the NIMSTIM face set (Tottenham et al., 2009); 24 faces (12 female) were selected. In an effort
to reect the race and ethnicity demographics of the Greater Boston Area 50% are Caucasian, 25%
are Asian/other, and 25% are African American (retrieved August 13, 2009 from http://www.
helloboston.com/Census.Cfm). We chose to use open-mouth angry face stimuli as they are
more reliably identied as angry than the closed-mouth angry stimuli (Tottenham et al.,
2009). Similarly, we chose to use angry faces because they are more reliably identied correctly
than fear faces (Tottenham et al., 2009). Each face is shown in both an angry expression and a
neutral expression, totaling 48 face stimuli. Face photographs were made uniform by centering
thefaceina1.68 ×2.42 boxwithablackbackground.
The task consists of 288 trials; 96 in each of the three cue types. Each trial begins
with a xation cross for 400 ms, followed by one of the four cue types presented for
100 ms, followed by an interval of 400 ms after which one of the three target stimuli
(neutral line anker, neutral face anker, angry face anker) is presented for
1700 ms or until the subject responds. The task was presented on an IBM ThinkPad
laptop computer using e-prime professional version 2.0.
2.4. Data analysis
Data analysis was conducted with SPSS 18.0. All variables were screened for normalcy
and outliers, dened as 2.5 or more standard deviations away from the mean of each group.
Outliers were replaced with the group mean accordingly. Eight scores were replaced: ve
ANT scores (four high SA), and three ANT-Emotion scores (one high SA). Independent t-
tests and χ
2
analyses were used to assess group differences on demographic variables. Uni-
variate Analysis of Variance (ANOVAs) and Multivariate Analysis of Covariance (MANCO-
VAs) were used to assess group differences on the ANT and ANT-Emotion. Pearson
correlations and linear regressions were calculated to assess the proposed mediation
model between SA, executive control of emotional information, and social functioning.
3. Results
3.1. Hypothesis 1: compared to controls, high SA participants will exhibit
attentional decits on both the ANT, specically in the executive control
network, and the ANT-Emotion, specically in the executive control of
emotional information
Attention network scores and test statistics for group differences on
the ANT are presented in Table 2. Due to group differences in IQ, IQ was
entered as a covariate of no interest in all analyses. Results showed that
there was no difference between high SA and control participants on
any of the ANT scores. Specically, ANOVAs revealed no group differ-
ences in overall reaction times [F(1,54)= 0.397, P =0.531] or accuracy
[F(1,54)=0.036, P =0.85]. MANCOVA with attention network scores
of the ANT (alerting, orienting, executive control) as dependent
variables revealed no main effect of group [F(3,52)=0.767, P=0.518]
or IQ [F(3,52)=0.563, P=0.642]. Similarly, follow-up ANOVAs
revealed no group differences on alerting [F(1,54)=2.373, P=0.129],
orienting [F(1,54)=0.42, P=0.839], or executive control network
scores [F(1,54)=0.127, P= 0.723]. Given that low IQ is a characteristic
feature of schizophrenia liability (Woodberry et al., 2008), removing
variance associated with IQ might be removing meaningful variance as-
sociated with the illness-related decit under investigation (Miller and
Chapman, 2009). Therefore, we also conducted these analyses without
IQ as a covariate; results remained the same. Thus, our hypothesis
that high SA individuals would exhibit decits in the executive control
network for non-emotional information was not supported (see Fig. 2).
Group means and test statistics for the ANT-Emotion are pre-
sented in Table 2. IQ was entered in all analyses as a covariate of no
interest. Results showed a single group difference in executive control
of emotional information, and no group differences on any other vari-
ables. Specically, ANOVAs revealed no group differences in overall
reaction times [F(1,59)= 0.343, P =0.56], accuracy [F(1,59)= 0.001,
P= 0.976], or orienting to emotional information [F(1,59)= 0.139,
P= 0.71]. There were, however, group differences in executive con-
trol of emotional information: compared to controls, high SA partici-
pants were signicantly slower to respond in the angry face anker
condition versus the neutral face anker condition [F(1,59) =5.478,
P= 0.023] (see Fig. 3). To examine whether this effect was driven
by differences in IQ we conducted these analyses without IQ as a co-
variate. Results remained the same: compared to controls, high SA
participants showed impaired executive control of emotional infor-
mation [F(1,60)= 3.971, P= 0.05].
GiventhatthetwogroupsnotonlydifferedonSA,butalsoonSPQ
scores (see Table 1), it is possible that other aspects of psychosis-
proneness contribute to this group difference in executive control of
emotional information. However, although SPQ scores did relate to SA
(r=0.76, Pb 0.0001) and social impairments (r=0.52, Pb 0.0001),
there was no signicant relationship with executive control of emotional
information (r= 0.02, P= 0.89). This indicates that the group differ-
ence in executive control of emotional information is not driven by
other schizotypal traits that are measured in the SPQ.
Collectively these ndings demonstrate that while high SA partici-
pants do not exhibit attentional decits in relation to non-emotional in-
formation, they do exhibit a specicdecit in the executive control of
emotional information. Moreover, this decit appears to be driven by
SA, rather than psychosis-proneness more generally.
3.2. Hypothesis 2: high SA individuals will report poorer social functioning
compared to controls
Mean social functioning and group differences are displayed in
Table 1. Consistent with our hypothesis, independent t-tests revealed
high SA participants reported signicantly poorer social functioning than
controls [t(59)= 4.245, Pb 0.0001]. This replicates previous ndings that
Table 1
Demographics and sample characteristics.
Control group High SA
group
Differences
between groups
N 29 34
Gender (F/M) 20 F/9 M 19 F/15 M χ
2
(1)=1.136, P = 0.287
Age: mean (S.D.), [range] 28.76 (13.81),[1865] 30.47 (14.04),[1964] t(61)=0.486, P = 0.629
Education: mean (S.D.), [range] 14.86 (2.01), [12 20] 14.53 (2.16), [1020] t(60)=0.612, P = 0.543
WASI IQ: mean (S.D.), [range] 119.52 (10.77), [92137] 111.76 (11.89), [82132] t(61)=2.692, P = 0.009, d =0.69
a
Social anhedonia: mean (S.D.), [range] 6.21 (3.82), [014] 26.85 (6.41), [1840] t(61)=15.184, P b 0.0001, d = 3.89
SPQ: mean (S.D.), [range] 19.97 (9.56), [940] 41.06 (15.47), [11 70] t(61) =6.372, P b 0.0001, d=1.63
Social impairment: mean (S.D.), [range] 56.30 (11.67), [3684] 70.68 (14.19), [39109] t(59)=4.245, P b 0.0001, d = 1.11
b
a
Cohen's d effect size.
b
Two subjects did not complete the Social Adjustment Scale.
31L.M. Tully et al. / Psychiatry Research 197 (2012) 2935
high SA is associated with poorer social functioning (Blanchard et al.,
1998; Cohen et al., 2006).
3.3. Hypotheses 3: executive control of emotional information will mediate
the relationship between social anhedonia and social functioning
Following the steps required for determining mediation (see
Baron and Kenny, 1986), we conducted a series of correlation and
regression analyses across all 63 participants to determine if there
were signicant associations between 1) SA and social functioning,
2) SA and executive control of emotional information, 3) executive
control of emotional information and social functioning, and 4) SA
and social functioning whilst controlling for executive control of emo-
tional information. All four steps must be met for a mediation model
to be supported. A variable is considered a statistical mediator if the
relationship between the independent (i.e. SA) and the dependent
400msa)
b)
+
-OR-
CUE
100ms
+
400ms
+
TARGET DISPLAY
1700ms
+
+
400ms
+
CUE
100ms
+
400ms
+
TARGET DISPLAY
1700ms
+
-OR-
+
Fig. 1. a: Illustration of an ANT-Emotion trial assessing orienting to emotional information. Participants see a neutral or angry face cue followed by a target arrow anked with neutral
lines. Scores for orienting to emotional information are obtained through simple subtractions of RTs: RT angry face cue RT neutral face cue. Lower scores indicate an orienting bias to
negative emotional faces. b: Illustration of an ANT-Emotion trial assessing executive control of emotional information. Participants see an asterisk cue followed by a target arrow anked
by neutral or angry faces. Scores for executive control of emotional information are obtained through simple subtractions of RTs: RT angry face ankers RT neutral face ankers. Higher
scores indicate reduced ability to inhibit negative emotional faces.
32 L.M. Tully et al. / Psychiatry Research 197 (2012) 2935
(i.e. social functioning) variable is signicantly reduced when the me-
diator (i.e. executive control of emotional information) is controlled
for (Baron and Kenny, 1986). Pearson correlations revealed social anhe-
donia correlated signicantly with social impairment (r =0.59;
Pb 0.0001), but executive control of emotional information did not corre-
late signicantly with either social anhedonia (r= 0.21, P=0.1) or social
impairment (r= 0.17, P= 0.19). Linear regression revealed social an-
hedonia signicantly predicted social functioning [F(1,59)=31.215,
Pb 0.0001; R
2
=0.35] such that higher social anhedonia predicted great-
er social impairment, satisfying step 1 of the mediation model. However,
social anhedonia did not signicantly predict executive control of emo-
tional information [F(1,60)=2.741, P=0.103; R
2
=0.04]. Similarly,
executive control of emotional information did not signicantly predict
social functioning [F(1,58)=1.803, P = 0.185; R
2
=0.03]. Thus, the me-
diation model was not supported. These non-signicant ndings could
be due to a small sample size; power analysis indicates that our sample
size has sufcient power to detect large and medium effects (0.99 and
0.70 respectively), but low power to detect small effects (0.12).
4. Discussion
This study examined social functioning and executive control of
emotional information in individuals at risk for developing schizo-
phrenia. Attentional processes were assessed using the ANT and our
new measure of executive control of emotional information, the
ANT-Emotion. Two main ndings emerged: rst, while there were
no group differences in alerting, orienting, or executive control net-
works assessed by the ANT, high SA individuals did exhibit a specic
impairment in the executive control of emotional information rela-
tive to controls. Second, high SA individuals reported signicantly
greater social functioning impairments relative to controls.
These ndings suggest that there are specicdecits in the execu-
tive control of emotional information observable in individuals with
vulnerability factors for schizophrenia. This decit was only apparent
in the presence of irrelevant angry faces, and not in the executive con-
trol network assessed by the ANT. This suggests that high SA individuals'
executive control may be intact but vulnerable, such that decits are not
detected by pure cognitive tasks, rather they only emerge when affec-
tive and cognitive information interacts. Moreover, high SA participants
did not exhibit faster orienting to emotional information indicating that
their slower reaction times in the presence of angry face ankers is not
simply due to an orienting bias towards angry faces. We interpret these
ndings as indicating that the impaired ability to inhibit emotional
information allows negative affective stimuli to exert inappropriate in-
uence on cognitive processes. This is consistent with prior studies indi-
cating that schizophrenia patients have an impaired ability to regulate
the inuence of irrelevant negative affective information on cognitive
Table 2
Attention network RT scores and accuracy of high SA and control participants.
Control group High SA group Differences between groups
ANT: mean (S.D.)
Alerting 33.98 (19.25) 42.88 (23.49) F(1,54) = 2.373, P=0.129
a
Orienting 46.30 (25.88) 49.55 (26.84) F(1,54) = 0.42, P = 0.839
Executive control 114.18 (40.31) 112.75 (41.76) F(1,54) = 0.127, P=0.723
Overall RT 549.42 (70.23) 566.72 (72.12) F(1,54) = 0.397, P=0.531
Accuracy (%) 97.53 (2.24) 97.53 (4.49) F(1,54)=0.036, P = 0.850
ANT-Emotion: mean (S.D.)
Executive control of emotional information 0.76 (16.98) 7.85 (16.86) F(1,59) = 5.478, P =0.023, η
ρ
2
=0.085
b,c,d
Orienting to emotional information 0.03 (15.07) 0.04 (17.40) F(1,59) =0.139, P =0.71
Overall RT 520.87 (73.1) 541.59 (88.14) F(1,59) =0.343, P = 0.56
Accuracy (%) 95.92 (2.86) 95.99 (2.53) F (1,59) =0.001, P = 0.976
a
Six control participants did not complete the ANT.
b
η
ρ
2
=partial eta squared effect size.
c
IQ was entered as a covariate of no interest. There was no main effect of IQ. Results remained the same in all analyses when IQ was not entered as a covariate.
d
One subject did not complete the ANT-Emotion.
Fig. 2. There were no differences between control and high SA participants on any of
the three attentional networks of the ANT, indicating that high SA is not characterized
by attentional decits in relation to nonemotional stimuli.
Fig. 3. High SA participants demonstrated impaired executive control of emotional
information: compared to control participants, high SA participants were signicantly
slower to respond to the target in the angry face anker condition versus the neutral
face anker condition.
33L.M. Tully et al. / Psychiatry Research 197 (2012) 2935
processes: patients show increased latencies on the emotional Stroop
(Bentall and Kaney, 1989), and rate faces as less trustworthy following
negative affective primes (Hooker et al., 2011). Moreover, this impair-
ment may be specically associated with SA: Suslow et al. (2003) exam-
ined the inuence of subliminal affective face primes on valence
judgments of neutral Chinese characters in schizophrenia patients with
and without SA. Compared to patients without SA, high SA patients
showed persistent negative evaluative shifts, indicating that impaired
regulation of irrelevant negative affect may be characteristic of high SA.
Our results are consistent with this, and indicate that it may also be char-
acteristic of individuals at risk for developing schizophrenia.
Our ndings also suggest that the decit in executive control may
be specic to the inhibition of socially relevant emotional informa-
tion. Using the emotion Stroop with non-socially specic negative
words, Mohanty et al. (2008) did not nd inhibitory decits in SA.
However, our ndings, and those of Suslow et al. (2003), suggest
that there is a decit in the presence of socially relevant stimuli (i.e.
negative emotional faces). This could contribute to the social
withdrawal and dysfunction characteristic of high SA: if individuals
struggle to inhibit socially relevant negative affective information, it
follows that they would withdraw from unnecessarily unpleasant
experiences (Suslow et al., 2003). Future studies could examine this
hypothesis further by adapting the ANT-Emotion to contain both so-
cial and non-social ankers, or by using an emotional Stroop with
categories of social and non-social negative words.
Consistent with our second hypothesis, high SA related to poorer
social functioning. This replicates previous ndings that high SA is as-
sociated with social impairments (Blanchard et al., 1998; Cohen et al.,
2006), providing further evidence for the presence of social decits in
people at increased risk for schizophrenia. However, executive control
of emotional information did not mediate the relationship between SA
and social functioning. There are two possible explanations for this.
First, it could be that there is a mismatch between the specicity of
the domain measured by the ANT-Emotion and the broad assessment
of social functioning obtained by the SAS-SR. We chose the SAS-SR be-
cause it is a standard measure used in the eld. However, like many so-
cial functioning assessments, it is broad in scope. Our nding suggests
that developing measures of social functioning that more accurately re-
ect the underlying social cognitive processes necessary for successful
social interactions may result in more success in revealing any underly-
ing relationship between SA, social cognitive decits, and social impair-
ments. Second, although our sample size is appropriate to detect
mediation of large and medium effects, it is not big enough to detect
small effects. Future research should examine the relationship between
executive control of emotional information and social functioning using
alternate measures of social impairments in sample sizes large enough
to detect small effects.
Several limitations of the current study should be acknowledged.
First, the ANT-Emotion is a newly created task; replications in inde-
pendent samples are needed and improvements may be warranted.
Of particular interest is the effect of stimulus onset asynchrony
(SOA). Unlike the ANT, the ANT-Emotion uses a constant SOA
(400 ms). This might allow participants to predict the onset of target
stimuli, possibly masking any orienting biases that might exist in the
sample, or even reducing group differences on executive control of
emotional information. However, despite these potential improve-
ments, the task provides valid and compelling data that high SA indi-
viduals have impaired executive control of emotional information.
The ANT-Emotion is based on the ANT a well-validated and reliable
measure of attention networks, of which the executive control piece
is based on another well-validated task the Eriksen anker
(Eriksen and Eriksen, 1974). Furthermore, the interference effect of
irrelevant affective information has been established in other tasks
such as the emotional Stroop, therefore it is unlikely that our ndings
are a consequence of an invalid task. A second limitation is that the
ANT-Emotion currently only uses angry faces, hence it is unclear if
our ndings would generalize to other facial expressions, both nega-
tive and positive. In light of the anhedonia paradox (Horan et al.,
2008), which suggests that the anticipation of reward, not consum-
mation, is the primary decit in schizophrenia, the relationship be-
tween SA and the regulation of positive emotional information is of
particular interest. Our ndings indicate that high SA is associated
with difculties regulating negative affective information and could
suggest a complementary decit in the facilitation of positive affec-
tive information, thought to underlie the observed decit in anticipa-
tory pleasure in anhedonia (Pizzagalli, 2010). Future studies could
examine both inhibitory and facilitatory mechanisms in the context of
emotional information and SA to delineate this further. Finally, there
were group differences on the SPQ. Although these differences are
expected given the close relationship between positive and negative as-
pects of schizotypy (Wuthrich and Bates, 2006), and they were shown to
have no impact on the group differences in executive control of emo-
tional information, future studies could investigate the specicinuence
of different aspects of psychosis-proneness on executive control of emo-
tional information.
In summary, the current study demonstrates a decit in the execu-
tive control of socially relevant emotional information in socially anhe-
donic individuals. Additionally, SA predicted poorer social functioning,
consistent with the idea that social impairments are a core characteristic
of psychosis-prone populations (Meehl, 1962). These ndings have im-
plications for how high-risk populations process negative affective infor-
mation in social contexts. Further research is needed to identify the
precise nature of these decits, and how they might contribute to the so-
cial dysfunction characteristic of schizophrenia.
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    • "All participants gave written informed consent in accordance to the guidelines provided by the IRB at Harvard University. To assess social, emotion and reward processing, participants completed laboratory assessments and self-reported questionnaires including the Temporal Experience of Pleasure Scale (TEPS; Gard et al., 2006), the Managing Emotions (ME) subscale of the Mayer–Salovey–Caruso Emotional Intelligence Test (MSCEIT-ME; Mayer et al., 2003), the Attentional Network Task-Emotion version (ANT-E; Tully et al., 2012), and the Global Functioning: Social scale (GF: Social; Cornblatt et al., 2007). The TEPS is a self-report questionnaire that includes consummatory and anticipatory subscales measuring trait tendencies in experiencing and anticipating pleasure (Gard et al., 2006); statements such as " The smell of freshly cut grass is enjoyable to me " (consummatory) and " When something exciting is coming up in my life, I really look forward to it " (anticipatory) are rated on a 1–6 Likert scale with higher scores indicating more hedonic responses. "
    [Show abstract] [Hide abstract] ABSTRACT: Social anhedonia (SA) is a debilitating characteristic of schizophrenia, a common feature in individuals at psychosis-risk, and a vulnerability for developing schizophrenia-spectrum disorders. Prior work (Hooker et al., 2014) revealed neural deficits in the ventral lateral prefrontal cortex (VLPFC) when processing positive social cues in a community sample of people with high SA. Lower VLPFC neural activity was related to more severe self-reported schizophrenia-spectrum symptoms as well as the exacerbation of symptoms after social stress. In the current study, psycho-physiological interaction (PPI) analysis was applied to further investigate the neural mechanisms mediated by the VLPFC during emotion processing. PPI analysis revealed that, compared to low SA controls, participants with high SA exhibited reduced connectivity between the VLPFC and the motor cortex, the inferior parietal and the posterior temporal regions when viewing socially positive (relative to neutral) emotions. Across all participants, VLPFC connectivity correlated with behavioral and self-reported measures of attentional control, emotion management, and reward processing. Our results suggest that impairments to the VLPFC mediated neural circuitry underlie the cognitive and emotional deficits associated with social anhedonia, and may serve as neural targets for prevention and treatment of schizophrenia-spectrum disorders.
    Full-text · Article · Aug 2015
    • "However, despite evidence demonstrating attentional control deficits in SA, the impact of these deficits on social functioning is rarely considered. In our previous work, we found high SA individuals demonstrated deficits in the attentional control of emotion information on an experimental task specifically designed to assess the ability to inhibit task-incongruent irrelevant negative faces, but these deficits did not relate to social impairments (Tully et al., 2012). However, highly specific experimental tasks may be too narrow to capture the effect of attentional control on social functioning. "
    [Show abstract] [Hide abstract] ABSTRACT: Social anhedonia (SA), a trait-like disinterest in social contact and diminished capacity to experience pleasure from social interactions, is consistently associated with social impairments in both healthy and clinical populations. However, the mechanisms underlying the relationship between SA and social impairment are poorly understood. Attentional control, selecting and focusing on relevant information and inhibiting irrelevant, may be one such mechanism. We examined individual differences in SA, attentional control, and social impairment in 108 healthy adults. High SA related to low attentional control and high social impairment. Moreover, attentional control mediated the relationship between SA and social impairment, establishing attentional control as one mechanism underlying aberrations in the fundamental human need for social contact. Although both attentional deficits and social impairment have been separately noted in SA, the relationship between SA, attentional control and social impairment in this non-clinical sample reflects a novel contribution.
    Full-text · Article · Dec 2014
    • "Studies using ECA paradigms present similar findings. PP individuals demonstrate impaired inhibition of irrelevant negative faces during a flanker task [63] , and increased negative word interference on the emotional Stroop task [95]. Similarly, GHR individuals show increased emotion interference effects on working memory performance, particularly in male subjects [96], and on emotional Stroop tasks [97]. "
    [Show abstract] [Hide abstract] ABSTRACT: The past 20 years of research examining psychosis risk factors has predominantly focused on “cold” cognitive (i.e., non-affective) processes. Despite identification of potential cognitive and associated brain-based vulnerability markers, our ability to identify those individuals at highest risk for future psychosis has not substantially improved. Consequently, researchers have begun to examine emotion processing deficits as potential psychosis vulnerability markers. Here we propose that a particular emotion processing domain, cognitive control of emotion, is a potential transdiagnostic mechanism underlying the heterogeneity of clinical presentation and psychosocial impairments observed in high-risk populations. Recent investigations indicate impaired cognitive control of emotion is observable across the psychosis spectrum and relates to important clinical and psychosocial outcomes relevant to the high-risk state. Moreover, preliminary evidence indicates treatment interventions aimed at improving cognitive control of emotion could reduce psychotic symptoms and improve functioning. We highlight gaps in current knowledge and propose five key avenues for future investigations.
    Full-text · Article · Sep 2014
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