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Psychiatry Research 219 (2014) 268–274

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Psychiatry Research
journal homepage: www.elsevier.com/locate/psychres

Neurocognitive predictors of social cognition in remitted schizophrenia


Urvakhsh Meherwan Mehta a,n, Haralahalli D. Bhagyavathi a, Jagadisha Thirthalli a,
Keshav J. Kumar b, Bangalore N. Gangadhar a
a
Department of Psychiatry, National Institute of Mental Health & Neurosciences (NIMHANS), Bangalore, India
b
Department of Clinical Psychology, National Institute of Mental Health & Neurosciences (NIMHANS), Bangalore, India

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

Article history: Knowledge of how specific neurocognition (NC) abilities predict social cognition (SC) in schizophrenia
Received 25 September 2013 has potential to guide novel integrated cognitive-remediation therapies. The scope of studies conducted
Received in revised form in this field is limited as they have not examined a comprehensive set of SC domains and they employ
21 May 2014
small sample sizes of heterogeneous patient groups. We studied a broad range of NC (sustained
Accepted 30 May 2014
Available online 7 June 2014
attention, processing speed, verbal/visual memory and visual processing/encoding, cognitive flexibility
and planning) and SC [different levels of theory of mind (ToM)], attributional bias, emotion recognition
Keywords: and social perception] abilities in 170 remitted schizophrenia patients. Multivariate regression analyses
Cognitive therapy revealed attention and planning as predictors of 1st order ToM. Memory encoding was the strongest
Theory of mind
predictor of 2nd order ToM. Faux-pas recognition, social perception and emotion recognition were
Social perception
influenced by a combination of cognitive flexibility and memory encoding abilities. Overall, NC predicted
Memory
Executive function anywhere between  4% and 40% of variance observed in specific SC sub-dimensions of attributional bias
(4%), 1st order (19%) and 2nd order (12%) theory of mind, faux-pas recognition (28%), social perception
(29%) and emotion recognition (39%). Individual SC abilities are predicted by distinctive as well as shared
NC abilities. These findings have important implications for integrated cognitive remediation.
& 2014 Elsevier Ireland Ltd. All rights reserved.

1. Introduction identify social roles, rules and contexts, as well as, make causal
attributions of social events that have personal relevance.
Deficits in social functioning, including interacting with others, Though NC and SC have been observed to exist as distinct
sustaining gainful employment and functioning in the community, cognitive constructs (Sergi et al., 2007; van Hooren et al., 2008;
are a defining feature of schizophrenia, making it a leading cause Mehta et al., 2013b), an average of about 10% of shared variance
of disability worldwide (Murray and Lopez, 1997). Impairments exists between these two constructs (Ventura et al., 2013). NC and
across a range of cognitive abilities predict these deficits in social SC together account for about a quarter of the variance in
functioning. Neurocognition (NC) involves general information functional outcomes in schizophrenia (Fett et al., 2011). Specifi-
acquiring and processing abilities. Attention, processing speed, cally, social cognition mediates the influence of neurocognition on
verbal and visual learning and memory, working memory and functional outcome (Schmidt et al., 2011). These findings have lead
reasoning and problem solving are the neurocognitive functions to the development of several cognitive remediation programs
impaired in schizophrenia (Green et al., 2004). Social cognition that target improvement in social and neurocognition, with the
(SC) includes specific mental operations underlying social interac- aim of translating this improvement to better functional outcomes
tions. SC domains studied in schizophrenia include theory of mind (Medalia and Saperstein, 2013). Results of these interventions
(ToM), emotion processing, social perception and knowledge and reveal benefits of small to moderate effect size in cognition and
attributional bias (Green et al., 2008). These processes involve an functional outcome (Wykes et al., 2011). Coordinated and inte-
inter-subjective quality, requiring reflective (meta-cognitive) and grated strategies that target enhancement of both neurocognition
social inferential abilities to infer thoughts and emotions of others, and social cognition have evolved over the years (Brenner et al.,
1992; Hogarty et al., 2004).
In keeping with the findings that SC mediates the influence of
NC on functional outcomes, emerging empirical evidence from
n
Corresponding author. Tel.: þ 91 80 26995250; Mobile: þ 91 9448208167; longitudinal studies suggests that NC underlies, and is causally
fax: þ91 80 26564830/26562121.
E-mail addresses: Urvakhsh@gmail.com (U.M. Mehta),
primary to SC (Hoe et al., 2012). Investigators have explored the
shaanbhagya@gmail.com (H.D. Bhagyavathi), jagatth@yahoo.com (J. Thirthalli), relationship between NC and SC—a recent meta-analysis suggest-
keshavjk@yahoo.com (K.J. Kumar), kalyanybg@yahoo.com (B.N. Gangadhar). ing small to medium range non-specific correlations among

http://dx.doi.org/10.1016/j.psychres.2014.05.055
0165-1781/& 2014 Elsevier Ireland Ltd. All rights reserved.
U.M. Mehta et al. / Psychiatry Research 219 (2014) 268–274 269

different dimensions of these two constructs (Ventura et al., 2013). typical antipsychotic medications, with mean chlorpromazine equivalents of
398.767 218.83 mg/day (Andreasen et al., 2010).
However, most of these studies report only correlation analyses
without controlling for the confounding effects of multiple NC
2.1. Assessments
predictors. Nevertheless, it appears intuitive that basic NC abilities
such as memory, executive functions and processing speed, among
Schizophrenia patients and healthy comparison subjects underwent assess-
others, may underlie rapid interpretation of complex social stimuli
ments for SC performance. In addition, the patients were assessed for their
to inform the moment-to-moment generation, refinement and neurocognitive performance and symptom status.
selection of models for thoughts and emotions of others, which
underlie diverse SC abilities. 2.1.1. Social cognition
Only a few studies have assessed specific neurocognitive Consistent with recommendations of the Measurement and Treatment
predictors of social cognition, by controlling for influence of other Research to Improve Cognition in Schizophrenia (MATRICS) New Approaches
cognitive predictors. A global neurocognitive index was found to Conference (Green et al., 2005) and the National Institute of Mental Health
sponsored meeting “Social Cognition in Schizophrenia: Basic Definitions, Methods
influence 1st order ToM abilities in a group of 36 symptomatic of Assessment, and Research Opportunities” (Green et al., 2008), we selected
schizophrenia patients (Bozikas et al., 2011). In a similar study on 4 domains of SC. Theory of Mind (ToM), social perception and attributional bias
43 clinically stable schizophrenia patients, none of the NC mea- were assessed using the Social Cognition Rating Tools in Indian Setting (SOCRATIS)
sures predicted 1st order ToM abilities, but executive functions (Mehta et al., 2011). Emotion processing was assessed using the Tool for Recogni-
tion of Emotions in Neuropsychiatric Disorders (TRENDS) (Behere et al., 2008).
from the WAIS-III had a significant influence on 2nd order ToM
abilities (Fernandez-Gonzalo et al., 2013). Early visual processing,
2.1.1.1. Theory of mind. Story-based tasks examined the ability, at different com-
and not other cognitive abilities like attention and working
plexity levels, to ‘meta-represent’ mental states of others (e.g., Suresh thinks that
memory was found to have a significant association with emotion Rani will go to the temple area to buy the ice-cream because she has not seen the
recognition and social perception (Kee et al., 1998; Sergi et al., ice-cream man go towards the school). The 1st, 2nd and higher order (faux pas)
2006) in schizophrenia. There are very few studies that have indices (see below) differentiated schizophrenia patients from healthy controls (-
explored the influence of NC on attributional bias in schizophrenia. known groups validity) with effect sizes (Cohen's d) ranging from 1.1 to 2.3 (Mehta
et al., 2011).
One such study found verbal IQ to be the only significant cognitive
measure to predict externalizing bias (Donohoe et al., 2008).
(a) 1st order ToM: This assesses the subject's ability to infer mental states of
Overall, these studies in patients with schizophrenia have pro- another person (i.e., the capacity to infer “A believes that x”). Tasks included
vided results that are inconsistent and non-specific. Limitations of two false-belief stories [based on Sally–Anne (Wimmer and Perner, 1983) and
these studies include small sample sizes, limited measurement of SC Smarties (Perner et al., 1987) tasks], and two metaphor detection stories (Drury
et al., 1998) since metaphor detection is considered to be a 1st order ToM
and NC abilities, lack of controlling for multiple NC abilities and
function (Brüne, 2005; Mehta et al., 2013a).
heterogeneous patient populations. Patients who have remitted from (b) 2nd order ToM: This assesses the subject's ability to infer what one person—
their positive symptoms may require cognitive remediation to over- other than the self infers about another person's mental states (i.e., the capacity
come the subtle residual cognitive and negative symptoms, which to infer “A believes that B believes that x”). Tasks included two false belief
influence their functional outcomes (Mehta et al., 2014). Interest- picture stories [based on ice-cream van (Perner and Wimmer, 1985) and
missing cookies (Stone et al., 1998) tasks], and two irony detection stories
ingly, schizophrenia patients in remission also demonstrate substan-
(Drury et al., 1998), since irony detection is considered to be a 2nd order ToM
tial impairments across diverse dimensions of SC abilities (Bora et al., function (Brüne, 2005; Mehta et al., 2013a).
2009; Mehta et al., 2013a), thus suggesting that SC deficits are likely (c) Higher order ToM: Ten stories to identify unintended social blunders or faux pas
trait-markers of schizophrenia. (five stories) or non-faux pas control situations (five stories) were used [based
on the faux pas recognition test (Stone et al., 1998)]. Faux pas recognition is
We aimed to explore the general cognitive predictors of four
described as a higher order ToM ability (Brüne, 2005). It involves the ability to
social cognition dimensions (theory of mind, emotion processing, understand a situation in which one person should have held information from
social perception and attributional bias) using multiple linear another, but did not. In addition to mental state attribution (i.e., purely ToM), it
regression models in a homogeneous group of remitted schizo- taps affective processing (Freedman and Stuss, 2011) as well—for instance,
phrenia patients. some clarifying questions assess how a person in the story felt during the faux
pas (Pijnenborg et al., 2013). In this background, faux pas scores were
considered separately and were not combined with the 1st and 2nd order
ToM scores for analyses.

2. Methods

2.1.1.2. Social perception. A set of 18 true/false questions were asked on social (e.g.,
Data for this analysis were obtained from a larger study to determine the Ali asked many questions about the movie because he was trying to impress Sunil)
clinical significance of SC ability in remitted schizophrenia patients (Mehta et al., and non-social cues (e.g., Harish and Lakshmi were looking over a book together)
2013a), conducted at the National Institute of Mental Health and Neurosciences, after showing the subjects four each of low and high emotion videos depicting a
Bangalore. The institute's ethics committee approved the study, which was social interaction. This test was adapted from the social cue recognition test
performed in accordance with the ethical standards laid down in the 1964 (Corrigan and Green, 1993). Apart from satisfactory content and known groups v-
Declaration of Helsinki and its later amendments. All patients provided written alidity, it had satisfactory internal consistency (Cronbach's alpha ¼ 0.78 across the
informed consent. eight videos) and concurrent validity (Intra-class correlation or the total scores in
A total of 170 consenting schizophrenia patients diagnosed independently by English and modified versions 4 0.7 for social cues) (Mehta et al., 2011).
two qualified psychiatrists according to DSM IV criteria, and confirmed using the
Mini-International Neuropsychiatric Interview (M.I.N.I.) (Sheehan et al., 1998) were
recruited. They fulfilled operational criteria for remission (scoring r 3 on Positive 2.1.1.3. Emotion processing. Facial emotion recognition ability was assessed using 52
and Negative Syndrome Scale (PANSS) rated for previous 6 months) in psychotic static images and 28 dynamic videos portraying two different intensities (low and
(P1-delusions, P3-hallucinatory behavior and G9-unusual thought content) and high) of six basic human emotions (happy, sad, fear, anger, surprise and disgust) de-
disorganization (P2-conceptual disorganization and G5-mannerisms/posturing) picted by four trained actors (one young male, one young female, one older male and
dimensions according to the proposed multidimensional criteria for symptomatic one older female). The TRENDS had satisfactory inter-rater reliability and internal c-
remission by “The Remission in Schizophrenia Working Group” (Andreasen et al., onsistency (Cronbach's alpha 0.45 for dynamic videos and 0.67 for static images)
2005). Patients with substance dependence in the last six months (except nicotine), (Behere et al., 2008).
and those with co-morbid neurological or medical disorder or clinically diagno-
sable or self-reported visual or auditory impairment were excluded. Those with a
score of r 19 on the Hindi Mental Status Examination (Ganguli et al., 1995) were 2.1.1.4. Attributional bias. This was assessed using a 32-point questionnaire where
excluded. All patients were on stabilized doses of anti-psychotics 4 months prior to subjects were required to make causal attributions for positive and negative social
evaluation. 150 (88.2%) patients were on atypical antipsychotics, nine (5.3%) were events, adapted from the Internal, Personal, and Situational Attributions Question-
on typical antipsychotics and the rest (6.5%) were on a combination of atypical and naire (Kinderman and Bentall, 1996). Apart from satisfactory content and known
270 U.M. Mehta et al. / Psychiatry Research 219 (2014) 268–274

groups validity, this test also had satisfactory internal consistency (Cronbach's al- (18.5) months. A substantial proportion (40.6%) of them belonged
pha ranging from 0.71 in schizophrenia patients to 0.87 in healthy volunteers) to the lower socioeconomic strata, defined according to possession
(Mehta et al., 2011).
of a below poverty line ration card provided by the government.
The SOCRATIS and TRENDS have been validated for use in the Indian cultural
Their mean (S.D.) positive and negative symptom scores on PANSS
setting with satisfactory psychometrics in terms of internal validity (see above)
(Behere et al., 2008; Mehta et al., 2011), as well as external validity (for SOCRATIS) were 7.61(1.2) and 11.35(4.8) respectively. SC and NC performance
by means of its associations with broader domains of empathy (r ¼ 0.45, p o 0.001) of a subset of these patients (n ¼ 60) was compared to that of
(Mehta and Thirthalli, 2014). Each test except the attributional biases provides an matched healthy subjects in a previous study (Mehta et al., 2013a).
index of the respective test performance, which is equivalent to the score of an Patients had deficits in all SC sub-dimensions even after control-
individual on the test divided by the maximum score possible (Mehta et al., 2011).
Externalizing bias was calculated by subtracting the number of negative events, for
ling for their neurocognitive deficits.
which the subject made internal attributes from the number of positive events. A
positive EB score represented the tendency to attribute negative events to external
3.2. Correlation analysis among SC and NC measures
causes. Personalizing bias was calculated as a ratio between the number of negative
events, for which the subject attributes to people, and the total number of negative
events for which the subject made external attributes. A score over 0.5 would Table 1 depicts Pearson's correlation coefficients between
indicate a tendency to attribute negative events to people rather than situations. different SC and NC measures; Table 2 shows the correlation
(Kinderman and Bentall, 1996). Hence, we had seven final scores that were used in
analysis within multiple SC dimensions assessed. Both attribu-
the analysis, namely, 1st order ToM, 2nd order ToM, faux pas recognition, social
perception and emotion recognition indices, and externalizing and personalizing tional bias scores had poor correlation with most of the NC
bias scores. measures. The other SC sub-domain scores had significant correla-
Based on recommendations of expert panels (Green et al., 2005, 2008), we tions ranging from 0.17 to 0.56 with various NC measures.
decided to group our outcome variables as theory of mind, emotion processing,
social perception and attributional bias. Furthermore, for the theory of mind
domain, we used the classification provided by Baron-Cohen (1995) and Brüne 3.3. Specific NC predictors of different SC sub-dimensions
(2005), which is based on the ontogeny of ToM in developing children. This system
classifies ToM as 1st order, 2nd order and higher order (e.g., faux pas identification). Forward multiple regression analyses were performed sepa-
rately, with each of the SC sub-domain scores (1st and 2nd order
2.1.2. Neuro-cognition ToM indices, faux pas composite index, emotion recognition index
Standardized tests were used from the National Institute of Mental Health and
and social perception index) as dependent variables. The NC
Neurosciences Neuro-psychological battery to assess sustained attention and
cognitive flexibility (color trails A and B respectively (D’Elia et al., 1994)), speed of measures that had a significant (p o0.05) correlation with these
processing (Digit Symbol Substitution Test (Wechsler, 1981)), verbal learning and SC measures were entered as independent variables. None of the
memory (Rey's Auditory Verbal Learning Test (Rey, 1941)), visuo-spatial construction independent variables in the regression model had variance
and visual learning and memory (Rey-Osterrieth Complex Figure Test (Osterrieth,
inflation factor Z2 (Zuur et al., 2010). The two attributional bias
1944)), visual processing and memory encoding (Benton Visual Retention Test
(Benton, 1974)) and planning (Tower of London test (Shallice, 1982)). These
scores had a single NC correlate, and hence were not used in
cognitive dimensions were chosen to resemble recommendations of the MATRICS regression analyses. The results of these regression analyses are
initiative (Green et al., 2004). The color trails difference score (B minus A) was also described in Table 3. 1st order ToM was predicted by sustained
used in the analyses as it is thought to correct for processing speed and yield a attention, planning and visual processing and encoding. Verbal
more sensitive measure for prefrontal functioning (Drane et al., 2002).
and visual memory encoding predicted 2nd order ToM. Cognitive
flexibility and verbal and visual memory encoding predicted faux
2.1.3. Symptom assessment
pas recognition as well as social perception. Cognitive flexibility,
Positive and Negative Syndrome Scale (PANSS) (Kay et al., 1987) was used to
define “remission” status and to assess psychopathology of the subjects. Two raters visual processing and encoding and speed of processing abilities
administered PANSS on patients after receiving adequate training in PANSS predicted emotion processing. Executive functioning (planning)
administration through training videos. All the assessments were completed on was associated with both the attributional bias measures. Overall,
the same day, in divided sessions. NC predicted  4–40% of variance observed in specific SC sub-
dimensions of attributional bias (4%), 1st order (19%) and 2nd
2.2. Statistical analysis order (12%) theory of mind, faux-pas recognition (28%), social
perception (29%) and emotion recognition (39%).
The data were analyzed using the Statistical Package for Social Scientists,
version 15.0 (SPSS, Chicago, IL). Seven outcome variables, representing the four SC
dimensions, were selected: 1st and 2nd order ToM indices, faux pas recognition
index, emotion recognition index, and social perception index, externalizing bias 4. Discussion
and personalizing bias. Pearson's correlation analysis was performed to examine
the association between different NC and SC scores. The neurocognitive measures
In this study, we aimed at exploring the neurocognitive pre-
which had a significant correlation (po 0.05) with specific SC outcome variables
were included in a forward multiple linear regression analysis. dictors of specific SC abilities: different levels of theory of mind,
attributional bias, emotion recognition and social perception—in
remitted schizophrenia patients. This would enhance our under-
3. Results standing of how general cognitive abilities influence complex
social information processing. Such knowledge would provide
3.1. Clinical and demographic details of the patients empirical evidence to guide integrated cognitive remediation
therapies to target individual SC domains through remediation of
All the 170 schizophrenia patients [49 (  29%) females] com- the basic neurocognitive abilities. Data from 170 remitted schizo-
pleted the required cognitive assessments. They had a mean (S.D.) phrenia patients were analyzed. Neurocognitive dimensions
age and education of 32.68 (9.26) and10.08 (2.52) years respec- assessed were processing speed, sustained attention, cognitive
tively. 97 (57.1%) of them were married, 4 (2.4%) were divorced and flexibility, planning, visual processing and encoding, and verbal
the rest were single. 19 (11.2%) patients were unemployed, the rest and visual learning and memory. Univariate statistics revealed
were homemakers, students or gainfully employed. 127 (74.7%) significant correlations among most of the NC and SC measures
patients had a diagnosis of paranoid schizophrenia; 30 (17.64%) assessed. However, the relationship between NC and attributional
had undifferentiated schizophrenia and 13 (7.64%) had schizoaf- bias was restricted, with only one measure of executive function
fective disorder. Their mean (S.D.) duration of illness was 91.31 having a significant association with both the externalizing and
(76.61) months and duration of symptom remission was 16.01 personalizing bias scores.
U.M. Mehta et al. / Psychiatry Research 219 (2014) 268–274 271

Table 1
Pearson's correlation analysis of SC and NC performance (n ¼170).

1st order ToM index 2nd order ToM index FPC index Emotion recognition index Social perception index EB PB

Color trails A time  0.324nn  0.252nn  0.401nn  0.510nn  0.451nn  0.081 0.105
Color trails B time  0.314nn  0.202nn  0.489nn  0.561nn  0.489nn  0.071 0.113
Color trails (B–A) time  0.252nn  0.139  0.388nn  0.492nn  0.425nn  0.053 0.098
AVLT total 0.165n 0.283nn 0.369nn 0.281nn 0.354nn 0.086  0.145
AVLT immediate recall 0.130 0.187n 0.360nn 0.198nn 0.322nn  0.010  0.087
AVLT delayed recall 0.139 0.208nn 0.357nn 0.245nn 0.314nn  0.010  0.092
CFT construction 0.297nn 0.043 0.373nn 0.434nn 0.345nn  0.035 0.007
CFT immediate recall 0.277nn 0.311nn 0.449nn 0.408nn 0.437nn 0.119  0.020
CFT delayed recall 0.298nn 0.270nn 0.445nn 0.412nn 0.436nn 0.136 0.025
Digit symbol substitution time  0.264nn  0.131  0.420nn  0.527nn  0.435nn  0.094 0.108
Tower of London time  0.145  0.019  0.176n  0.131  0.231nn 0.109 0.010
Tower of London moves  0.132 0.117  0.029 0.110 0.011 0.113 0.005
Tower of London NPSMM 0.318nn 0.102 0.260nn 0.201nn 0.223nn  0.173n  0.185n
BVRT immediate recall 0.347nn 0.222nn 0.373nn 0.503nn 0.380nn 0.124  0.033

ToM ¼ theory of mind, FPC ¼ faux pas composite, EB¼ externalizing bias, PB¼ personalizing bias, NPSMM ¼number of problems solved with minimum moves,
AVLT¼ Auditory Verbal Learning Test, CFT ¼ Complex Figure Test, BVRT¼ Benton Visual Retention Test, B–A represents the difference between the two color trail time scores.
n
po 0.05.
nn
p o0.01

Table 2
Pearson's correlation (r) matrix for social cognition sub-scores (n¼ 170).

1st order ToM index 2nd order ToM index FPC index ER index SP index EB PB

1st order ToM index 1


2nd order ToM index 0.321nn 1
FPCI 0.365nn 0.263nn 1
ER index 0.345nn 0.188n 0.513nn 1
SP index 0.347nn 0.265nn 0.536nn 0.517nn 1
EB  0.043 0.113 0.029 0.158n 0.1 1
PB  0.109 0.087  0.074  0.03  0.06 0.027 1

ToM¼ theory of mind, FPC ¼ faux pas composite, ER ¼ emotion recognition, SP ¼ social perception, EB¼ externalizing bias, PB¼ personalizing bias
n
p o0.05.
nn
p o 0.01

Regression analyses with 1st order ToM as the dependent differences in functional outcome measures, patterns of brain
variable revealed executive functions and visual memory encoding activation or other indices of validity in schizophrenia.
as significant predictors. This suggests that information acquiring, Higher social cognitive processes like faux pas recognition and
processing and storing, as well as ability to look-ahead, generate social perception showed common neuropsychological correlates.
goals and plan forward represented by bilateral prefrontal (Rowe Both executive functions and memory encoding processes predicted
et al., 2001; Lesh et al., 2011) and medial temporal lobe (Lepage these SC processes, accounting for about 29% of the total variance.
et al., 1998) functions could underlie 1st order ToM. Both verbal The prefrontal and medial temporal lobes might collectively con-
and visual memory predicted 2nd order ToM. The encoding and tribute to such higher social cognitive processes. Cognitive flexibility
retrieval processes involved in memory and influenced by cogni- and visual processing and encoding predicted the emotion-
tive control, are supported by complimentary functions of the processing dimension of SC. Lastly, both the attribution bias scores
medial temporal (perirhinal cortex and hippocampus) and pre- had significant correlations with executive functions only.
frontal (ventrolateral and dorsolateral) lobes (Ranganath et al., Examination of the magnitude of variance in SC explained by
2008). This finding is consistent with previous reports associating NC processes revealed a range varying from 4% to 40%. The
mentalizing deficits with deficits in different aspects of memory, increase in explained variance for each significant NC predictor
not just in schizophrenia (Corcoran and Frith, 2003), but across of SC was substantial and significant (Table 3). Division of SC
different patient subgroups (Zobel et al., 2010; Sayin et al., 2010) as dimensions based on the magnitude of variance explained by NC
well as healthy individuals (Ciaramelli et al., 2013). These findings partially maps on to the three SC factors identified in an earlier
also support the view that we use memory of our past experiences exploratory factor analysis (Mancuso et al., 2011). Maximal influence
to draw inferences about the mental states of others and simulate (29–39%) of NC was on emotion recognition, social perception and
how they feel (Mitchell, 2009). Executive functions have also been faux-pas recognition. A common aspect in these three SC dimensions
shown to be associated with 2nd order ToM in schizophrenia was that each of them required a component of affect-driven
(Fernandez-Gonzalo et al., 2013). Cognitive flexibility and planning processing of presented stimuli. These included detecting emotions
were the executive functions assessed in this study. However, the through facial expressions (emotion recognition) (Behere et al.,
combined contribution of verbal and visual memory was greater 2008), social cues (social perception) (Corrigan and Green, 1993),
than that of executive functions in predicting 2nd order ToM. In and mental state attribution (faux pas) (Freedman and Stuss, 2011;
this context, it is important to understand that even though the Pijnenborg et al., 2013). Interestingly, the social cue detection factor
ontogenetic framework of classifying ToM (Baron-Cohen, 1995; identified by Mancuso et al. (2011) also had loadings from facial
Brüne, 2005) describes three distinct levels, the validity of these emotion recognition, social perception and lie detection. There was
levels has not been established by specific links to meaningful moderate influence (12–19%) of NC on both the 1st and 2nd order
272 U.M. Mehta et al. / Psychiatry Research 219 (2014) 268–274

Table 3
Regression analysis for specific neurocognitive predictors of social cognition sub-domains.

Dependent variable Predictors β t p VIF Adjusted R2 R2 change F change

1st order theory of mind index (F¼ 14.03, p o 0.001) BVRT Immediate recall 0.203 2.58 0.011 1.29 0.115 – –
Tower of London NPSMM 0.222 3.06 0.003 1.09 0.164 0.054 10.83**
Color trails A time  0.188  2.42 0.016 1.25 0.188 0.03 5.9*
2nd order theory of mind index (F¼ 11.94, p o 0.001) CFT immediate recall 0.234 2.93 0.004 1.20 0.091 – –
AVLT total 0.186 2.33 0.021 1.20 0.115 0.03 5.5*
Faux pas composite index (F ¼21.89, po 0.001) CFT immediate recall 0.249 3.07 0.003 1.52 0.197 – –
Color trails B time  0.237  2.97 0.003 1.47 0.245 0.054 11.9**
AVLT immediate recall 0.189 2.63 0.009 1.19 0.284 0.04 7.1**
Emotion recognition index (F ¼36.86, p o 0.001) Color trails B time  0.310  3.77 o 0.001 1.86 0.311 – –
BVRT immediate recall 0.244 3.34 0.001 1.47 0.373 0.065 17.56**
Digit symbol substitution time  0.195  2.33 0.021 1.93 0.389 0.02 5.44*
Social perception index (F¼ 24.25, p o 0.001) Color trails B time  0.324  4.171 o 0.001 1.44 0.235 – –
CFT delayed recall 0.204 2.609 0.01 1.46 0.275 0.044 10.2**
AVLT total 0.161 2.264 0.025 1.21 0.292 0.021 5.1*

β ¼standardized coefficients, VIF ¼ variance inflation factor, ToM¼ theory of mind, NPSMM ¼ number of problems solved with minimum moves, AVLT ¼ Auditory Verbal
Learning Test, CFT ¼Complex Figure Test, BVRT¼ Benton Visual Retention Test, significance at
n
po 0.05;
nn
p o0.01

ToM abilities. These SC functions as assessed using the test batteries the ratings of the two raters was not established. Finally, it should
used in this study, tapped predominantly inferential processes be noted that results from longitudinal studies are better suited to
requiring subjects to make deductions about thoughts, beliefs and determine the neurocognitive basis of social cognitive deficits.
actions in relatively affect neutral situations. Indeed, Mancuso's Our patients were all remitted from positive and disorganiza-
inferential and regulatory processing factor also had loadings from tion symptoms. It is during symptomatic remission, that the role of
sarcasm detection, which involves mental state attributions additional recovery oriented therapeutic interventions like cogni-
(Mancuso et al., 2011). There was very little influence (2–4%) of NC tive remediation becomes necessary. Hence, these findings may
in predicting attributional bias. Mancuso et al. (2011) identified closely translate to real world settings in which cognitive reme-
hostile attributional style as the third SC factor in their study. The diation strategies are feasible. Moreover, demonstrating these
relatively poor relationship between attributional bias scores and NC associations in a relatively homogeneous patient population
measures is reflective of the school of thought that attributional bias reflects a relationship closer to reality, free of effects of symptoms.
is a divergent cognitive style rather than a deficit in cognitive ability Nevertheless, we acknowledge that these results can be general-
(Mizrahi et al., 2008). It also suggests that attributional bias may be ized only to patients who have remitted from their positive
relatively independent of basic neurocognitive processes, unlike symptoms. In our knowledge, this is the first study to explore
other SC sub-dimensions. specific NC predictors of a range of recommended SC abilities in
Important caveats need to be considered while interpreting schizophrenia.
these results. We have used a broad range of NC measures, which To conclude, executive functions and memory, especially its
include all dimensions recommended by the MATRICS initiative encoding component, have specific associations with different SC
(Green et al., 2004) except specific tests of working memory and abilities in patients with remitted schizophrenia. This could
attention. It should be noted that the Tower of London and trail potentially reflect the contribution of the prefrontal and medial
making B tests, which were used to measure executive functions, temporal lobes in such processes. Though evidence supports
have substantial contribution of working memory as well (Welsh distinctiveness of NC and SC, there exists a relative independence.
et al., 1999; Sanchez-Cubillo et al., 2009; Nuechterlein et al., 2011). Our findings reveal that NC predicts anywhere between 4% and
Moreover, Trail making-A gives a measure of attention, in addition 40% of variance observed in specific SC sub-dimensions. Emotion-
to speed of processing (Reitan and Wolfson, 1985). Nevertheless, driven processes like emotion recognition, social perception and
we do not rule out the possibility that inclusion of working faux pas recognition had the strongest association with NC, while
memory/sustained attention in the NC battery could have altered attribution bias had the least association with NC. These findings
the results. The absence of a healthy comparison group to study provide empirical evidence that would be valuable in guiding
the differences in NC/SC performance when compared to schizo- integrated cognitive remediation therapies.
phrenia patients and their differential interactions in the two
groups limits generalization of the study findings. However, SC
performance of 60/170 patients reported in this study was com-
Conflict of interest
pared to age, gender and education matched healthy controls in an
earlier study. This revealed that patients had substantial SC deficits
Drs. Mehta, Bhagyavathi, Thirthalli, Kumar and Gangadhar
even after controlling for NC across all dimensions (Mehta et al.,
report no biomedical financial interests or potential conflicts of
2013a). Our study is based on the grounds of a hierarchical
interest.
relationship between NC and SC. That is to say, that neurocogni-
tion is elementary and underlies SC (Hoe et al., 2012). Never-
theless, recent studies suggest that a bidirectional relationship
between NC and SC may also be possible. This is based on the Acknowledgments
findings that social cognitive training may benefit neurocognition
as well (Lindenmayer et al., 2013). In addition, there is a possibility We acknowledge and thank the Indian Council of Medical
of our results being influenced by sensitivity differences between Research MD financial assistance award 2007–2009 (No. 3/2/
different NC and SC measures (e.g., test differences in difficulty 2008/PG-Thesis-MPD-29) for partially funding this study. The
level, floor and ceiling effects). The inter-rater reliability between ICMR had no further role in study design; in the collection,
U.M. Mehta et al. / Psychiatry Research 219 (2014) 268–274 273

analysis and interpretation of data; in writing of the report; and in 2004. Cognitive enhancement therapy for schizophrenia: effects of a 2-year
the decision to submit the paper for publication. randomized trial on cognition and behavior. Archives of General Psychiatry 61,
866–876.
Kay, S.R., Fiszbein, A., Opler, L.A., 1987. The positive and negative syndrome scale
(PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261–276.
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