Progress in Neuropsychopharmacology & Biological Psychiatry 94 (2019) 109672

Contents lists available at ScienceDirect

Progress in Neuropsychopharmacology
& Biological Psychiatry
journal homepage: www.elsevier.com/locate/pnp

Social cognition in psychosis: Predictors and effects of META-cognitive T

training
Aldara Alvarez-Astorgaa, Eva Soteloa, Alba Lubeirob, Rodrigo de Luisc, Javier Gomez-Pilard,
⁎
Begoña Becoecheaa, Vicente Molinaa,b,
a
Psychiatry Service, Clinical University Hospital of Valladolid, Valladolid, Spain
b
Psychiatry Department, School of Medicine, University of Valladolid, Spain
c
Imaging Processing Laboratory, University of Valladolid, Valladolid, Spain
d
Biomedical Engineering Group, University of Valladolid, Valladolid, Spain

A R T I C LE I N FO A B S T R A C T

Keywords: Social cognition deficits are found in schizophrenia and bipolar disorder, but its neural underpinnings are poorly
Schizophrenia understood. Given the complexity of psychological functions underlying this kind of cognition, we hypothesized
Social cognition that alterations in global structural connectivity could contribute to those deficits. To test this hypothesis, we
Fractional anisotropy studied a group of schizophrenia and bipolar patients with connectomics based on diffusion magnetic resonance
Prefrontal cortex
imaging and assessments of general and social cognition. The latter was assessed using the Mayer, Salovey and
Metacognitive training
Caruso Emotional Intelligence Test (MSCEIT) for emotional intelligence and the Spanish Group for
Schizophrenia Treatment Optimization (Grupo Español para la OPtimización del Tratamiento de la Esquizofrenia,
GEOPTE) test for behavioral aspects of social cognition. Graph theory applied to fractional anisotropy for the
connections among cortical regions was used to obtain the small-world (SW) index of the structural connectivity
network. In addition, we assessed the possibility of predicting the response of social cognition deficits to Meta-
cognitive Training based on their possible underpinnings in a subgroup of patients. Patients showed lower scores
in emotional intelligence and behavioral social cognition. MSCEIT scores were associated with SW index and
working memory, and GEOPTE scores were related to verbal memory. Improvement in social cognition after
Meta-cognitive Training was associated with lower scores of the social cognition in the baseline, according to the
GEOPTE scale. Our findings support structural connectivity as one of the factors underlying emotional in-
telligence in schizophrenia, and the use of Meta-cognitive Training to improve social cognition in patients with
larger deficits.

1. Introduction emotional intelligence, theory of mind and general cognition, at least.

Relevant roles in social cognition have been proposed at least for
Social cognition is defined as “the processes by which we draw in- medial frontal (Amodio and Frith, 2006), anterior cingulate cortex
ferences about other people's belief and intentions and how we weigh (Rushworth et al., 2007) and insular-frontotemporal network (Adolfi
social situational factors in making these inferences” (Green et al., et al., 2017). In this context, methods allowing describing the global
2008). Significant deficits in social cognition have been demonstrated properties of the cerebral network may be useful to assess the under-
in patients with schizophrenia (Savla et al., 2013), even in prodromal pinnings of social cognition. Among these, recent analyses using net-
stages (Lee et al., 2015), as well as first episode (Szmulewicz et al., work parameters derived from graph-theory have been used to describe
2019) and stable euthymic (Tatay-Manteiga et al., 2018) bipolar pa- global properties of the connective network in the brain in relation to
tients. Other authors reported lesser intensity in these deficits in bipolar cognition (van den Heuvel et al., 2009). Since fast coordination of many
patients (Bora and Pantelis, 2016). Social cognition influence functional different functions is likely required for a proper social cognition, and
outcomes in psychotic patients (Irani et al., 2012). network alterations have been reported in schizophrenia (Gomez-Pilar
The neural substrate of social cognition is likely complex, since this et al., 2018; van den Heuvel et al., 2010), a relationship between
kind of cognition involves a set of psychological functions, such as structural network dysconnectivity and social cognition deficits in

⁎
Corresponding author at: Dept. of Psychiatry, University Hospital of Valladolid, Av. Ramón y Cajal, 7, Valladolid 48005, Spain.
E-mail address: vicente.molina@uva.es (V. Molina).

https://doi.org/10.1016/j.pnpbp.2019.109672
Received 1 March 2019; Received in revised form 7 June 2019
Available online 19 June 2019
0278-5846/ © 2019 Elsevier Inc. All rights reserved.
A. Alvarez-Astorga, et al. Progress in Neuropsychopharmacology & Biological Psychiatry 94 (2019) 109672

Table 1
Demographic, clinical and cognitive values in the sample. Significant differences in comparison to healthy controls *p < .05; **p < .01; ***p < .001.
Patients Chronic SZ FE SZ Bipolar Healthy controls (n = 38)
(n = 79) (n = 37) (n = 19) (n = 23)

Sex 44:35 20:17 11:8 13:10 21:17

Age 37.5(11.6) 38.03(10.24) 29.50(9.19) 42.29(11.97) 36.37(11.62)
Treatment (CPZ eq) 287.0(224.3) 383.69(253.64) 348.21(184.61) 157.25(157.65) NA
Positive symptoms 10.6(3.8) 12.35(4.42) 11.15(2.64) 7.69(1.97) NA
Negative symptoms 14.2(6.0) 17.53(7.16) 14.46(2.93) 9.31(2.78) NA
Education (years) 14.6(3.7) 13.73(3.00) 15.38(3.50) 14.38(4.83) 16.50(3.10)
Father education (years) 11.8(3.9) 10.91(3.23) 13.36(4.17) 14.78(3,62) 15.33(8.62)
GEOPTE-patient (basal) 29.9(11.3)** 33.6(11.0)*** 25.25(11.1)** 27.7(10.6)*** 20.4(3.2)
GEOPTE-patient (post-MCT) 25.0(8.0) 26.4(8.9)** 19.7(4.1) 22.7(4.8) NA
GEOPTE-relatives (basal) 32.5(12.6)** 35,9(13.6) *** 30.9(13.4) *** 30.2(9.7) *** 19.4(3.2)
GEOPTE-relatives (post-MCT) 27.1(13.4) 33.5(13.4)*** 18.5(14.5) 19.7 NA
MSCEIT total 98.6(21.3)** 93.5(17.4) *** 100.9(19.9) ** 94.3(14.3) *** 120.1(12.9)
Verbal memory 35.3(10.8)*** 33,74(9,4) *** 39,1(8.7) ** 34,3 (13.4) *** 50,2(8.8)
Working memory 16.8(4.6)** 15,7(4.6) *** 17,3(4.3) ** 17,2(4.3) 24,1(2.2)
Motor speed 61.4(15.2)** 57,7(16.2) *** 59,2(11.6) ** 68,8(15.2) 86,2(10.0)
Verbal fluency 19.6(5.3)*** 19,7(4.9) *** 17,6(4.9) *** 21,2(6.1) 29,9(5.3)
Performance speed 42.8(14.4)*** 39,5(16.1) *** 50,69(12.7) ** 44,3(12.11) *** 70,0(19.3)
Problem solving 16.2(4.0)* 17,1(4.0) 15,2(4.5)* 15,6(3.6)* 17,2(2.8)
Total IQ 94.9(12.1) 94.03(12.74) ** 89.85(11.68) ** 99.33(10.93) ** 112.27(10.93)
SW index 0.977(0.011) 0.976(0.012) 0.981(0.006) 0.977(0.013) NA

schizophrenia can be proposed. schizophrenia, 19 first-episode (FE) schizophrenia and 23 euthymic

Previous reports have analyzed relations between local dysconnec- bipolar patients with a history of psychosis) and 38 healthy controls
tivity and social cognition in schizophrenia without global network (HC; Table1). Of them, 38 (26 Sz, 12 bipolar) patients underwent a
analyses, to the best of our knowledge. A recent report supports an cycle of Meta-cognitive Training (MCT) and their social cognition data
association between social cognition deficits (indirectly assessed by were re-assessed after this cycle.
means of the Scale for the Assessment of Negative Symptoms (SANS) Diffusion tensor imaging (DTI) and general cognition data were
and structural dysconnectivity between premotor cortex and, on the available in 50 patients (21 chronic and 13 FE schizophrenia and 16
other hand, anterior cingulate and inferior parietal regions in 16 first bipolar patients). Data from DTI were used to assess structural network
episode-schizophrenia patients (Saito et al., 2018). Fractional aniso- connectivity in patients to test the hypotheses of significant relation-
tropy (FA, a measurement reflecting integrity of white matter tracts) in ships between structural connectivity and (i) social cognition deficits in
the anterior cingulate was inversely associated with performance in an the patients and (ii) the response to MCT. Social cognition and DTI data
emotional attribution task (Fujiwara et al., 2007), likely associated with were acquired within the same month. In previous studies including
social cognition, too. these cases, we have compared structural connectivity between patients
We are not aware of any previous assessment of the relation be- and controls with different methodologies (Gomez-Pilar, de Luis-
tween global structural connectivity and direct measurements of social Garcia, 2018, Molina et al., 2019, Molina et al., 2017).
cognition. Given the interest of such relation in the psychotic syndrome Inclusion criteria for patients were: (i) schizophrenia or bipolar
(including affective and non-affective psychoses), we studied the asso- disorder diagnosis according the criteria in the Diagnostic and
ciation between performance in relevant dimensions of social cognition Statistical Manual of Mental Disorders, 5th edition, made by an expert
and global cerebral connectivity network parameters in schizophrenia clinician who was treating most of the cases (V.M.); and (ii) for the FE
and bipolar patients. We hypothesized a positive association between patients, illness duration of less than one year. Patients were recruited
social cognition scores and small-world (SW) index, a parameter sum- in the local day clinic (50) or mental health centers (29) between 2016,
marizing global brain connectivity through the balance between local March and 2018, November. Diagnoses were made using psychiatric
connectivity or specialization and the efficient communication between interviews and all the available information (clinical records, relatives'
distant brain regions. This way, SW is a measure of overall efficiency of information). All patients were on stable doses of atypical antipsychotic
the brain network. treatment. Psychotic symptoms were scored in all patients using the
Complementarily, we tested the possibility of predicting the im- Positive and Negative Syndrome Scale (PANSS) (Kay et al., 1987).
provement of social cognition deficits with psychosocial techniques Clinical data are shown in Table 1.
such as Meta-cognitive Training (MCT) (Wells, 2008) based on the Exclusion criteria were: (i) intelligent quotient under 70; (ii) past or
properties of the connective network and general cognition. This present substance abuse (except caffeine and nicotine); (ii) cranial
technique is useful in alleviating social cognitive deficits in psychosis trauma with loss of consciousness longer than one minute; (iv) for pa-
(Rocha and Queiros, 2013). We hypothesized that if a relation could be tients, any other mental or neurological diagnosis, and (v) for controls,
found between global connectivity and social cognition, connectivity any current neurological or psychiatric diagnosis or any treatment af-
deficits measured as the SW index might help in predicting response to fecting central nervous system.
MCT. Since social cognition deficits are found in both schizophrenia The study complied with the ethical standards of the Helsinki
and bipolar disorder, we studied the proposed relations in both syn- Declaration and was approved by the ethical committee of the
dromes together. University Hospital of Valladolid.

2. Subjects and methods 2.2. Cognitive assessment

2.1. Patients Global IQ was assessed using a Spanish brief version of the Wechsler
Adult Intelligence Scale WAIS-III (Fuentes Dura et al., 2010). We used
We assessed social cognition in 79 patients (37 of them chronic the Spanish version of Brief Assessment in Cognition in Schizophrenia

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A. Alvarez-Astorga, et al. Progress in Neuropsychopharmacology & Biological Psychiatry 94 (2019) 109672

Scale (BACS) (Segarra et al., 2011; Wheeler and Voineskos, 2014) to removal of non-brain structures. On the other hand, anatomically
assess performance in verbal memory (list learning), working memory constrained whole brain tractography was performed using the dMRI
(digit span), motor speed (token motor task), verbal fluency (cate- data, but also the anatomical images in order to guide the tractography
gories), attention and processing speed (symbol coding) and executive process. Also, from DTI, fractional anisotropy (FA) maps were obtained
function and problem solving (Tower of London). after estimating diffusion tensors for each voxel from the diffusion
Social cognition subsumes different specific (for instance, theory of weighted images. FA, which measures the degree of anisotropy of the
mind, emotional intelligence) and general (such as verbal fluency, diffusion tensor, is a well-known descriptor of white matter integrity
working memory and problem solving) psychological functions. We that has been widely employed in the literature.
assessed social cognition using the MSCEIT (Mayer et al., 2003) and Finally, connectivity matrices were computed from the tractography
GEOPTE (Grupo Español para la OPtimización del Tratamiento de la output and the (registered) gray matter segmentation. We defined 84
Esquizofrenia, GEOPTE) (Sanjuan et al., 2003) tools (see Supplemen- regions from FreeSurfer parcellation, therefore 84 × 84 connectivity
tary material). These are complementary instruments, since the MSCEIT matrices were obtained, and mean FA along each connection was em-
is aimed at assessing emotional intelligence and the GEOPTE scores ployed as a connectome metric.
relational and behavioral aspects. The MSCEIT includes faces, designs Throughout the entire processing pipeline, FSL (http://fsl.fmrib.ox.
and pictures to elicit emotions, as well as questions and judgements ac.uk), FreeSurfer (http://surfer.nmr.mgh.harvard.edu) and MRtrix
about hypothetical emotional, personal and social situations, yielding (www.mrtrix.org) were used as software tools.
scores in the dimensions of emotional perception, facilitation, under- From the structural connectivity matrices, SW was calculated for
standing and management. Some aspects assessed with the GEOPTE are each subject (Rubinov and Sporns, 2010). SW is a useful description of
difficulties in following conversations with several participants, re- the topology of the whole network, providing a measure of the network
cognizing emotions in others, interpreting their gestures, ability to efficiency. In order to define SW, clustering coefficient (CLC) and path
catch the meaning of conversations, or solving domestic problems, length (PL) need to be defined first. From them, SW is the ratio between
making week-end plans or establishing friendly relations. Using the CLC and PL, both normalized with respect to null-hypothesis networks
GEOPTE, changes in social behavior can be more readily scored, thus (Rubinov and Sporns, 2010). The corresponding mathematical for-
this instrument was selected for assessing changes after MCT. The mulae and definitions can be found in (Gomez-Pilar, de Luis-Garcia,
GEOPTE has the additional advantage of including scores from both 2018, Molina, Bachiller, 2018, Molina, Lubeiro, 2017).
patient and a relative.
2.5. Statistics
2.3. Metacognitive-training
We compared socio-demographical data (age, sex, subjects and
Metacognitive training was administered as a group therapy on parental education) and general cognition between patients and con-
semi-structured sessions aimed to address frequent cognitive bias that trols (t or χ2 tests when appropriate). Total MSCEIT and GEOPTE scores
may increase the likelihood of psychotic symptoms. This kind of in- (obtained from patients, GEOPTE-p, and from relatives, GEOPTE-r)
tervention addresses interpersonal (such as theory of mind) and in- were compared between patients and controls using t-tests.
trapersonal (such as jumping to conclusions) aspects likely related to We used a stepwise multivariate regression in order to assess pre-
social cognition deficit in psychoses. A cycle of MCT includes seven dictors of social cognition in the patients with MSCEIT and GEOPTE
modules (attributional styles, jumping to conclusion, beliefs, theory of scores as dependent variables, and BACS scores and SW index as pre-
mind, memory, and self-esteem). Each session, a module addressing one dictive variables in the regression. Since three regression analyses were
of these biases was developed, encouraging patients participation, ex- performed, p level was set at p = .016. Collinearity and homo-
perience sharing and vicarious learning. Complete information can be scedasticity were tested using tolerance statistics and the distribution of
found at https://clinical-neuropsychology.de/metacognitive_training- residuals. The relation between social cognition and illness duration
psychosis/ and treatment dosage (mg/d in chlorpromazine (in mg/d in CPZ)
equivalents) was explored using Pearson's correlations.
2.4. Diffusion MRI acquisition and processing To assess the prediction of social cognition deficits to MCT, we first
assessed its efficacy comparing GEOPTE scores from both patients and
Acquisition and processing of MRI images to obtain FA-based con- relatives before and after a cycle of such therapy using t-tests for related
nectivity values were performed as explained in more detail in previous samples. Then, we explored the possible correlates of improvement
reports (Gomez-Pilar, de Luis-Garcia, 2018, Molina, Bachiller, 2018, with this therapy using Pearson's correlations between change in
Molina, Lubeiro, 2017). Acquisitions were carried out using a Philips GEOPTE scores and, on the other hand, baseline GEOPTE scores, and
Achieva 3 Tesla MRI unit (Philips Healthcare, Best, The Netherlands) in general cognition and connectivity measurements found to be asso-
the MRI facility at Valladolid University, and were composed of T1- ciated to social cognition basal scores.
weighted and diffusion weighted images.
For the anatomical T1-weighted images, acquisition parameters 3. Results
included: Turbo Field Echo (TFE) sequence, matrix size of 256 × 256,
spatial resolution of 1 × 1 × 1 mm3 and 160 sagittal slices covering the There were not significant differences in age, sex distribution, or
whole brain. Echo time and repetition time were 3.7 and 8.1 ms, re- education years, between patients and controls, except for a younger
spectively, and flip angle was 8°. age in the FE patients. Patients showed a significant deficit in general
With regard to the diffusion weighted images, parameters were: 61 cognition (Table 1).
gradient directions, one baseline volume, b-value = 1000 s/mm2, Patients (n = 79) showed lower total MSCEIT (t = −5.78,
2 × 2 × 2 mm3 of voxel size, matrix size of 128 × 128 and 66 axial df = 120, p < .001) and higher GEOPTE (GEOPTE-p t = 5.095,
slices covering the entire brain. Total acquisition time was around df = 129, p < .001; GEOPTE-r t = 5.441, df = 101, p < .001) scores
18 min. than controls (Fig. S1). Lower MSCEIT and higher GEOPTE scores in-
Essentially, connectome matrices were created, for each subject, by dicate worse social cognition.
analyzing the white matter integrity of the fiber bundles connecting the In the patients (n = 50), total MSCEIT scores were positively pre-
considered gray matter regions. In order to do that, cortical and sub- dicted by working memory (β = 0.323) and SW index (β = 0.309; for
cortical gray matter structures were first segmented into 84 regions the model R2 = 0.228; df = 1,36; F = 5.16; p = .010; Fig. 1). Residuals
from the Desikan-Killiany atlas using the T1-weighted images after the were normally distributed, and tolerance was larger than 0.95 in all

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A. Alvarez-Astorga, et al. Progress in Neuropsychopharmacology & Biological Psychiatry 94 (2019) 109672

Fig. 1. In the upper row, scatterplots depicting the association between emotional intelligence (MSCEIT) scores and SW index of the structural connectivity network
and working memory. These two variables were selected as predictors of MSCEIT scores (R2 = 0.228, p = .010, see text). In the lower row, association between
verbal memory and behavioral social cognition. Verbal memory predicted GEOPTE-r scores at trend level (R2 = 0.167, p = .018, see text). Circles: chronic SZ, crosses
FE Sz, stars: bipolars.

cases. Thus, higher MSCEIT scores, indicating better emotional in- intelligence) were lower in psychotic patients as compared to healthy
telligence, were predicted by higher working memory scores and by controls. These scores were predicted by working memory performance
larger SW index of connective structure. and the SW index of the structural connectivity network. Behavioral
GEOPTE-p scores were not predicted by any variable combination. aspects of social cognition were associated with verbal memory.
GEOPTE-r scores were inversely predicted at trend level of significance The association between emotional intelligence and working
by verbal memory (β = −0.409; for the model R2 = 0.167; df = 1,32; memory might be coherent with a prefrontal role in social cognition,
F = 6.26; p = .018; Fig. 1). Thus, higher verbal memory predicted since working memory is intimately associated with prefrontal function
better social performance according to family perception. (Fuster, 1999). Moreover, this association also seems coherent with the
After MCT (n = 31), there was a significant improvement in social relation between social cognition and SW index. The SW structure of a
cognition as scored by the patients (GEOPTE-p; t = 4.43, p < .001) network, such as the brain, is characterized by a high density of local
and by relatives (GEOPTE-r, t = 2.00, p = .05; Table 1). connections and a smaller number of long-distance connections, con-
The change of GEOPTE-p scores with MCT (post-treatment minus verging in some highly connected nodes (hubs), such as the PFC, a
baseline scores) was inversely associated with basal GEOPTE-p scores region highly interconnected with many other regions. Thus, con-
(r = −0.604, p = .001; Fig. 2). This implies that patients with higher nectivity alterations at the PFC, may decrease the “small-worldness” of
baseline GEOPTE (i.e., worse social cognition) are more likely to benefit the global network (i.e., the degree in which this network approximates
from metacognitive therapy. to an ideal SW structure) and, therefore, its connective efficiency
which, according to our data, might hamper social cognition in schi-
4. Discussion zophrenia. Although we did not measure connectivity in particular re-
gions in this study, specific alterations in the structural connections of
In this sample, total MSCEIT scores (associated to emotional the PFC have been described in schizophrenia (Molina, Lubeiro, 2017),

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A. Alvarez-Astorga, et al. Progress in Neuropsychopharmacology & Biological Psychiatry 94 (2019) 109672

cognition, perhaps more pre-reflective. Social cognition scored with

GEOPTE was associated with verbal memory performance, more asso-
ciated with the medial temporal than to the prefrontal region.
MCT and similar techniques may be useful for alleviating social
cognitive deficits (Rocha and Queiros, 2013). Our results suggest that
this efficacy may be larger in patients with higher baseline deficits and
better problem-solving capacities. In our sample, the improvement in
GEOPTE-r scores supports a real-life effect for MCT. A randomized trial
showed efficacy for MCT for improving key components in social cog-
nitive deficits in schizophrenia, such as jumping to conclusions or
theory of mind (Ochoa et al., 2017). However, beyond baseline deficits,
we could not find other significant predictors (i.e., biological or cog-
nitive) of response to MCT, but our sample size was small.
Our study has limitations. The statistical power is small to draw
conclusions about the predictive value of structural connectivity for
improvements with MCT in social cognition. The MSCEIT gives relevant
information for social cognition, but does not cover other potentially
important aspects, such as perception from relevant others. Our sample
includes bipolar and schizophrenia patients and, although both show
social cognition deficits, specific differences may be found between
Fig. 2. Association between improvement in behavioral social cognition after
these syndromes, which can be addressed in future studies with larger
meta-cognitive therapy and baseline GEOPTE scores (r = −0.604, p = .001),
showing that larger baseline deficits (i.e., higher baseline scores) predict a samples. We have not included a comparison group to assess the MCT
larger improvement after MCT (i.e., more negative post-MCT minus baseline effects, but our goal in this respect was looking for response predictors.
scores). Circles: chronic SZ, crosses FE Sz, stars: bipolars. Finally, we have not assessed the possible relations between social
cognition and structural connectivity in healthy controls, which could
help interpreting the corresponding results in our patients.
in addition to the widely replicated anatomical and functional altera-
As a conclusion, our data support a role for structural dysconnec-
tions for this region in schizophrenia. The architecture of cerebral
tivity and general cognition in social cognition deficits in psychoses, as
connectivity has SW properties that optimize integrated cerebral func-
well as the efficacy of MCT in patients with larger social cognition
tion (Bassett et al., 2009, van den Heuvel, Stam, 2009), which seem
deficits.
disrupted in schizophrenia (Gomez-Pilar, de Luis-Garcia, 2018,
Micheloyannis et al., 2006, van den Heuvel, Mandl, 2010) and are
predictive of emotional intelligence in our sample. Contributors
In this context, the relation in our patients between working
memory, SW and emotional intelligence may be coherent with a lower V. Molina and R. de Luis-García designed the study and wrote the
efficiency of the global network, perhaps mediated by alterations in protocol. V. Molina performed clinical assessment. A. Lubeiro and R. de
prefrontal connectivity. In other words, the prediction of emotional Luis-García performed the image analysis. J. Gomez-Pilar computed the
intelligence in patients by working memory and SW index of con- graph measures. A. Alvarez and V. Molina undertook the statistical
nectivity is coherent with the possibility that PFC connectivity disrup- analyses and wrote the manuscript. E. Sotelo and performed the cog-
tions may contribute to social cognition deficits by disrupting the global nitive study. B. Becoechea carried out metacognitive therapy. All au-
connective network properties. thors contributed to the article, revised and approved the final manu-
In a sample overlapping with the present study, we recently re- script.
ported that the SW properties of the structural connectivity was de-
creased in both schizophrenia and bipolar patients (Cea-Canas et al.,
Role of the funding source
2019). This finding together with the present study, supports that an
alteration of the structural connectivity network may have a role in
This study has been supported by the Instituto de Salud Carlos III
social cognition deficits in both syndromes.
(PI18/00178) and the Gerencia Regional de Salud de Castilla y León
In our patients, GEOPTE-r scores were predicted by verbal memory,
(GRS 1485/A/17 and GRS 1721/A/18) grants to V. Molina.
although at trend level of significance, by verbal memory performance.
The funding sources had no role in the design or analyses of the
Verbal memory is highly related to temporal lobe, and the superior
study. Permission from these sources was not required for publication.
temporal gyrus is another important hub region with a key role in in-
All the authors approved the final draft.
tegrating sensory and emotional inputs (Brunelle et al., 2013). Volumes
of the superior temporal region and FA in the fronto-temporal part of
superior right fasciculus were associated with performance in a theory Ethical statement
of mind task (Cabinio et al., 2015). Therefore, it may be proposed that
alterations of temporal functions and/or connectivity may also con- The study complies with The Code of Ethics of the World Medical
tribute to a decreased SW index and hamper social cognitive capacities. Association (Declaration of Helsinki).
It is interesting that the associations with general cognition and After receiving full written information, subjects provided written
structural connectivity of emotional intelligence (scored with MSCEIT) consent. The ethical committee of the University Hospital of Valladolid
and the behavioral aspects of social cognition (scored with GEOPTE) approved the study.
were different, perhaps indicating different substrates. Emotional in- There are not conflicts of interest to declare for none of the authors
telligence showed a more evident relation with global efficient con- in relation to the present study.
nectivity, reflected in SW index, and with working memory, a basic
aspect of prefrontal cortex function (Fuster, 1999). This may indicate
Declaration of competing interests
that emotional intelligence requires a more widespread psychological
and cerebral involvement than behavioral manifestations of social
None of the authors has any conflict of interest to declare.

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Acknowledgements prodromal psychosis: a meta-analysis. Schizophr. Res. 164, 28–34.

Mayer, J.D., Salovey, P., Caruso, D.R., Sitarenios, G., 2003. Measuring emotional in-
telligence with the MSCEIT V2.0. Emotion. 3, 97–105.
We thank technicians in the MRI facility at Valladolid University for Micheloyannis, S., Pachou, E., Stam, C.J., Breakspear, M., Bitsios, P., Vourkas, M., et al.,
their kind collaboration in the acquisition of the images. 2006. Small-world networks and disturbed functional connectivity in schizophrenia.
Schizophr. Res. 87, 60–66.
Molina, V., Lubeiro, A., Soto, O., Rodriguez, M., Alvarez, A., Hernandez, R., et al., 2017.
Appendix A. Supplementary data Alterations in prefrontal connectivity in schizophrenia assessed using diffusion
magnetic resonance imaging. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 76,
Supplementary data to this article can be found online at https:// 107–115.
Molina, V., Bachiller, A., de Luis, R., Lubeiro, A., Poza, J., Hornero, R., et al., 2019 Jun.
doi.org/10.1016/j.pnpbp.2019.109672. Topography of activation deficits in schizophrenia during P300 task related to cog-
nition and structural connectivity. Eur. Arch. Psychiatry Clin. Neurosci. 269 (4),
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