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a
Neuropsychology Unit and Laboratory of Experimental Neuropsychology, Department of Neurology, Geneva
University Hospital, b Faculty of Psychology and Educational Science and c Department of Neuroscience, University
Medical Center (CMU), University of Geneva, Geneva, and d Neurology Unit, Department of Medicine, Faculty of
Key Words left CVAs were impaired in verbal/discourse tasks (social cog-
Clinical scale · Neuropsychological evaluation · Brain nition, inferences, absurd stories, and cartoons. Conclu-
damage · Social emotions · False beliefs · Inferences · sions: The GeSoCS is a medium duration assessment tool
Absurdity judgement · Executive planning that appears to detect and characterize significant social im-
pairment in neurological patients. © 2015 S. Karger AG, Basel
Abstract
Background: Social cognition is widely studied in neurolo-
gy. At present, such evaluations are designed for research or Introduction
for specific diseases and simple general clinical tools are
lacking. We propose a clinical evaluation tool for social cog- The last decade saw the development of social neuro-
nition, the Geneva Social Cognition Scale (GeSoCS). Meth- science, which integrated social psychology, cognitive
ods: The GeSoCS is a 100-point scale composed of 6 subtests neuropsychology and neurosciences and raised the ques-
(theory of mind stories, recognition of social emotions, false tion of whether social cognition exists as a specific do-
beliefs, inferences, absurdity judgement and planning abili- main (for review see Ward [1]). Social cognition refers to
ties) chosen from different validated tests of social and cog- the abilities and processes allowing people to interact and
nitive evaluation. Eighty-four patients with neurological dis- to understand the behaviour of others. Among these dif-
orders and 52 controls participated in the study. Evaluation ferent processes, the capacity to attribute mental states
duration lasted 20–60 min. Results: Mean scores were 92.6 ± such as feelings and beliefs and then to predict behaviour
4.5 for controls and 76.5 ± 15.3 for patients and differentiate is called theory of mind (ToM) and plays a determining
patients and controls in all subtests. With a cut-off score of role in social adaptation. ToM was first studied in pri-
84, the scale had a sensitivity of 62% and a specificity of 94%. mates [2], and subsequently in developmental psycholo-
In our stroke subgroup, right CVAs failed in cartoons, infer- gy [3]. Its first clinical application involved autistic per-
ences, ‘mind in the eyes’, and in the temporal rule task while sons [4]. Social cognition has also been addressed exten-
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E-Mail karger@karger.com
4, Gabrielle-Perret-Gentil, 1205 Geneva (Switzerland)
www.karger.com/ene
E-Mail mdmartory @ bluewin.ch
sively using brain imaging techniques. Along these lines, Table 1. Demographic characteristics of control and patient groups
fMRI studies, for example, have shown that the temporal
lobe, the temporal-parietal-junction, the medial prefron- Control group Patient group
(n = 52) (n = 84)
tal cortex and the posterior cingulate cortex are specifi-
cally involved in ToM [5–7]. Age, mean (SD) 42.2 (16.4) 53.3 (15.5)
In the field of clinical neuroscience, investigations of Gender
brain-injured patients with acute or neurodegenerative Male 20 49
Female 32 35
disease have also revealed different types of impairments Handedness
in social cognition and the understanding of people’s be- Right 51 71
haviour [8]. Indeed, ToM constitutes a complex domain Left 1 13
that involves numerous cognitive processes, including Level of education, years
executive functions [9, 10] and, in certain conditions, <12 1 11
>12 51 73
normal language development [11].
Thus, the evaluation of social cognition and ToM in
adults relies on a wide range of tasks of varying complex-
ity. The most common involves false beliefs and can be
used with young children. In particular, first-order beliefs Table 2. Patient group aetiologies
necessitate understanding another person’s mental state, Patient Stroke Trauma Tumor Dementia Encephalopathy
while second-order beliefs, which are more complex, pre- group (n = 31) (n = 17) (n = 7) (n = 17) (n = 11)
dict what a person thinks about a third person’s feelings (n = 84)
[3, 4]. More complex tasks used to assess the mental state
Age,
of others require that participants identify a person’s emo- mean
tional state on the basis of the expression in their eyes (the (SD) 58 (12.8) 41 (13) 51 (14) 66.4 (8.8) 44.8 (16.6)
‘mind in the eyes’ test) [12, 13], detect a social ‘faux pas’ Gender
Male 15 13 4 11 7
[14], or understand mental inferences or indirect speech Female 16 4 3 6 4
as in metaphors and jokes. Children are able to resolve Handedness
these tasks at different ages (age 4 for the first order false Right 28 14 6 14 8
belief and 9 or 11 for the faux pas). In brain-damaged pa- Left 3 3 1 3 3
tients, a number of authors have proposed that patients
with brain injuries would process simple false beliefs sto-
ries correctly but would fail in more complex tasks [14].
Despite the great number of studies in social neurosci- neurological patients rather than a short screening tool.
ence investigating patients with acute acquired or neuro- Deficits identified with this tool would then allow subse-
degenerative brain damage, research in the field has not quent detailed examination using the existing tests.
yet provided tests that are broad enough for use in the
clinic and have focused either on specific pathologies,
such as multiple sclerosis [15] or neurodegenerative
Method
groups (for review see Henry et al. [16]), or alternately,
have addressed specifics such as false beliefs [17], or faux Participants
pas recognition [14]. Additional global testing, as de- All subjects gave written informed consent for their participa-
scribed earlier, is often too long for clinical practice. To tion in accordance with the Declaration of Helsinki. The study was
our knowledge, there is yet no general test that allows approved by the local Ethics Committee, (Commission d’Ethique
de la Recherche Clinique, Geneva University Hospital, Switzerland;
neuropsychologists to assess ToM and social cognition CER 10-073).
function more globally in everyday clinical practice. The population was composed of 52 healthy French-speaking,
The aim of this study is thus to offer a short assessment volunteers, with no known neurological or psychiatric disorders.
tool that is easy to use in everyday neuropsychological Demographic data are summarized in table 1.
practice, which has been developed from existing tests de- Eighty-four brain-damaged French-speaking patients were ex-
amined consecutively during their hospitalization in the neuro-
scribed in the literature such as the mind in the eyes test logical clinic. The patient population presented various aetiologies
or false beliefs. This scale was intended as a clinical tool (stroke, epilepsy, trauma, tumour, dementia; table 2). Participants
for potential impairment in social cognition found in with CVA were assessed in the post-acute stage (about 10 days to
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3 weeks after their stroke and after stabilization for other aetiolo- Is Willy rather affectionate with his wife this evening? (response:
gies). All patients’ diagnoses were based on a clinical evaluation, a yes).
laboratory evaluation including an MRI, and a formal neuropsy- Tasks 5 and 6 are beyond ToM strictly speaking but are used to
chological assessment. Exclusion criteria included a history of pri- determine clinically a general executive impairment, which can be
or psychiatric disorders, delirium, global aphasia and severe de- associated (although not necessarily) with deficits in social cogni-
mentia (≥CDR3). tion [9].
Subsequent statistical inquiries as to the effects of levels of edu- Task 5 required that patients correctly detect an absurdity in
cation on our tests showed that this factor did not influence the 4 stories and accept a control story (e.g. ‘The management of a
results. The different levels were therefore merged. railroad company noticed that in train accidents, injuries were for
more serious in the tail wagons. Consequently, it was decided to
Assessment of ToM and Social Cognition remove the last wagon of each train. What do you think of that?’).
The test was developed internally on the basis of the literature This test was retained as it constituted an interesting match with
reported above and spanned aspects most frequently explored in the social cognition stories that also required a ‘meta’ representa-
social cognition. Each of them was evaluated through specific tasks tion, albeit without the social component (adapted from Binet and
as described in the literature and combined in order to form a scale Simon [22]).
with a total score of 100 points (online suppl. appendix, see www. Task 6 was not directly related to social cognition, but was pre-
karger.com/doi/10.1159/000442412). sented as a general measure of executive function. It is a French
Tasks 1, 2, 3 and 4 were specific to social cognition and com- adaptation of the Counter test [23] and consists in determining the
prehension of inferences. For each of them, the patients were asked rules underlying the temporal appearance of colour counters (e.g.
to read a story and to answer specific questions involving ToM, but black-white-white, black-white-white…). This test was chosen for
also to respond to simple control questions in order to test linguis- its ease of use and its good prediction of mental flexibility in fron-
tic comprehension. The lengths of the stories were similar. In ad- tal impairment [24].
dition, precautions were taken to ensure that the questions and the Every verbal or picture task contained control questions
syntactic structures of the sentences were equivalent and simple measuring literal comprehension but excluding ToM or social
enough to be understood by most patients. aspect. The control questions were not scored but were includ-
Task 1 was composed of 5 written ToM and social cognition ed to ensure correct linguistic comprehension. The item ‘Jim’
stories: one ‘faux pas’ situation, one ‘normal’ situation (‘Helen’ and that constituted a full question in the test was an exception. The
‘Jim’ stories [14]), one ToM story (‘burglar’ story [18]), and one duration of the whole test ranged from about 40 min in a
in-house ToM story involving a self-perspective1. healthy subject to between 60 and 70 min in the brain-damaged
Task 2 involved 10 items chosen from the ‘reading the mind in patients. In this latter group, participants could re-read the sto-
the eyes’ test [12, 13]. The original test is composed of 36 pairs of ries or obtain repetitions of the questions. Patients and control
eyes each evoking an emotion. The subject has to choose between subjects were examined by clinically qualified neuropsycholo-
4 written propositions the one that best describes the emotion. The gists.
items selected (1-4-5-8-14-16-18-30-33-35) were retained as being
the most easily identifiable on the basis of a pilot experiment with Procedure
25 participants. The Geneva Social Cognition Scale (GeSoCS) was tested in ad-
Task 3 was made up of 5 ToM picture stories [19] representing dition to the patients’ standard neuropsychological examination,
first- and second-order false beliefs (e.g. A man is sitting on a which will not be detailed in this study. In controls, no additional
bench with his dog beside him and he is preparing to eat a sand- evaluation was performed, as participants were considered to be
wich; while he is throwing the paper packaging, a bird steals the cognitively normal. However, a semi-structured interview was car-
sandwich; on seeing the sandwich missing, the man scolds the ried out to confirm the absence of any indicators of cognitive im-
dog. Question: why does the man scold his dog?) and one story pairment, either anamnestically or behaviourally. The subjects
not requiring inference (A boy sits on his sofa when he hears the were individually tested in a single session of about 40–60 min. The
doorbell ring. He thinks that it is the mailman but he smiles when sessions took place at the University Hospital of Geneva, in the
he sees that it is his friend. Question: Why does the boy seem Neuropsychology Unit.
happy?). During the test, they were asked to answer the questions freely
Task 4 was composed of 5 stories that the patient had to read and no solutions were proposed. If necessary, the question was re-
before answering questions about possible or impossible infer- peated. For each item, full points were given when the answer was
ences [20, 21] e.g. ‘The more Willy loses at the casino, the more complete and correct. Half points were given if the answer was in-
affectionate he is with his wife; apparently, he was not very lucky complete, or if the answer was correct but not the explanation.
in his game this evening’. Control question without inference:
Did Willy win a lot at the casino this evening? (response: no). Statistical Analysis
Question with impossible inference to make: Is Willy’s wife rich? The results of the whole group are described first, followed by
(response: we cannot know). Question with an inference to make: that of the patients and controls (global scores, then subtests).
Significant differences and interactions between the controls and
the patients were calculated using an analysis of variance
1
In a fMRI study with healthy subjects, Vogeley et al. [2001], found differ- (ANOVA; statistical analyses were performed using Statistica
ent patterns of brain activation, as the subjects took the first or third person 12 software). For the smaller and more heterogeneous groups
perspective and Gambini, Barbieri, Scarone [2004], supported this idea in a (TBI, dementia), additional testing was carried out using non-
study involving schizophrenic subjects. parametrical tests.
149.126.78.17 - 12/14/2015 5:44:51 PM
0.40
–0.40
Controls
Patients
Fig. 1. Comparison of mean z-scores of –0.80
controls and patients for all the tasks.
Results Table 3. Results: mean scores and SD for controls and patients for
all tasks
Descriptive statistics for the controls and the patients
Tasks Controls (n = 52), Patients (n = 84),
are provided in table 3. The controls obtained a total mean (SD) mean (SD)
mean score of 92.6/100 (SD 4.5); for each test, the result
was close to the maximum score with a standard devia- Social cognition 19.36 (1.20) 16.02 (4.08)
tion equal to 1, with the exception of the ‘mind in the eyes’ Mind in the eyes 15.09 (2.28) 12.11 (3.81)
test, (mean 15/20, SD 2.3). There was no significant dif- ToM cartoons 19.55 (0.79) 17.22 (3.5)
Inferences 19.17 (1.49) 15.83 (4.4)
ference due to gender (women 92.4, men 93). The pa- Absurd stories 9.65 (0.94) 7.78 (2.32)
tients obtained a total mean score lower than the controls Temporal rules 9.76 (0.85) 7.54 (3.42)
(76.51) with a large dispersal (SD 15.32) and performanc- Total 92.61 (4.51) 76.51 (15.32)
es for each test were lower than the controls.
For every task, the performance of the patients and the
controls were expressed as z-scores of the mean total
group’s performances (patients + controls; fig. 1). The ANOVA confirmed that the difference was sig-
An ANOVA comparing the 2 groups’ z-scores revealed nificant (F(15, 395) = 4.4,651, p < 0.05). However, when
a significant difference in performance between the con- considering the side of the lesion, a post hoc Fisher test
trols and the patients (F(1, 134) = 55.035, p < 0.00001), and showed different patterns of impairment in the case of
a post hoc test showed that the patients were impaired right CVA, left CVA or bilateral CVA.
compared to the healthy subjects in all tasks. Right CVAs did not differ from the controls in the first
We now considered the mean z-score for the CVA pop- task of social cognition and were quite correct in ‘faux pas’
ulation compared to the mean z-score of the control group. stories, which required criticism (p = 0.06), but they failed
in cartoons, in inferences and in tasks in which they had to
Comparison of z-Scores: CVA Patients vs. Controls guess a feeling, such as the ‘mind in the eyes’ test (p < 0.05),
The 31 patients with CVA demonstrated approxi- or an intention, such as in the temporal rule task (p < 0.05).
mately the same pattern as the entire patient group with Left CVAs were impaired in all verbal tasks, social cog-
altered performances compared to the controls as shown nition tasks (p < 0.05), inferences (p < 0.05), absurd sto-
in figure 2. ries, and also in cartoons (p < 0.05). Conversely, they have
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Controls ight C A eft C A ilateral C A
. 0
0.80
0.40
–0.40
Social cognition
Mind in the eyes
–0.80
Cartoons
Inferences
– . 0 Absurd stories
Temporal rules
Fig. 2. Comparison of mean z-scores of
right CVA, left CVA, bilateral CVA and – . 0
controls for all the tasks.
shown significant difficulties in the ‘mind in the eyes’ task Table 4. Cut-off for each subtest and the total test
(p = 0.07).
Finally, bilateral CVAs were significantly impaired Tasks Controls, Cut-off (rounded
mean (SD) to nearest unit)
(p < 0.05) in all 6 tasks.
Social cognition 19.36 (1.20) 17
Determining Pathological Function: The Cut-Off Score Mind in the eyes 15.09 (2.28) 11
Based on these data, we attempted to determine a cut- ToM cartoons 19.55 (0.79) 18
Inferences 19.17 (1.49) 16
off score for clinical use. The values for each test are given Absurd stories 9.65 (0.94) 8
in table 4 using a cut-off score of minus 2 SDs. Temporal rules 9.76 (0.85) 8
Using these values, 52 patients fell below the cut-off Total 92.61 (4.51) 84
(84) and 32 remained above; among the 31 CVA patients,
19 were below the cut off (9/15 left, 5/8 right and 5/7 bi-
lateral CVA); 3 healthy subjects fell below the cut-off and
49 were above. The cut-off of 84 allowed to significantly rological patients in a daily clinical practice. This screening
differentiate between controls and patients (χ2(1) = 42.02; test was constructed with items taken from existing tasks
p < 0.0001). Sensitivity was at 61.9% and specificity at previously described in the literature for evaluating the
94.23%. An analysis computing the receiver operating ToM. These tasks were subsequently adapted and grouped
curve (ROC) with these cut-off scores showed an esti- in order to form a scale graded from 0 to 100. To the best of
mated area of 0.78 under the curve. Thus, the probability our knowledge, it is the first global tool adapted for every-
of correctly classifying a neurological patient as patho- day clinical work as most of the studies on clinical patients
logical on the basis of our test is 78% (fig. 3). until now have used extensive batteries. From a clinical per-
spective, GeSoCS appears to conform to the criteria for a
consistent scale. First, the GeSoCS uses multiple aspects of
Discussion validated tests for assessment of ToM, a ‘complex, multi-
faceted cognitive ability’ [25]. On average, GeSoCS lasts
In order to provide a simple tool for evaluating social 40–60 min. Generally, this duration is easily tolerated by
cognition, we designed the GeSoCS, which allows rapid neurological patients, although one cannot exclude poten-
and easy assessment of social cognition in hospitalized neu- tial attentional deficits during evaluation.
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tients those who have effectively a deficit in social cogni- task while left CVAs were impaired in verbal/discourse
tion. As mentioned, the high specificity allows predicting tasks (social cognition, inferences, absurd stories, and
that impaired results at the GeSoCS in neurological pa- cartoons). Furthermore, we did not attempt any qualita-
tients are indeed related to the disease and less probably tive analysis of the answers or the different questions for
to non-neurological effects and are a sign of an acquired social cognition (ToM, point of view, faux pas) and did
deficit in social cognition. In order to confirm the eco- not establish correlations between the GeSoCS and neu-
logical validity of the GeSoCs, we made a post hoc corre- ropsychological (e.g. executive functions and language)
lation between the GeSoCS scores and scores obtained at or ecological measures. Finally, the test was intended to
the dysexecutive questionnaire (DEX) [31], a standard- be as short as possible and thus, the test samples used may
ized 20 items rating scale used for quantifying behav- not have had the same diagnostic value as the test as a
ioural disturbances commonly associated with executive whole, e.g. the ‘reading the mind in the eyes’ test consists
impairment. In an unselected subgroup of 28 patients, a of 36 items, but only 10 were selected for our task.
close relative completed the DEX questionnaire. In this More elaborate studies on the different patient groups
subgroup, there was a correlation between total GeSoCS should be considered and, in particular, their correlation
score and DEX score (CC = –0.450, p = 0.02). with other ecological measures, including questionnaires
Another limitation of this study is the fact that various and behavioural scales, could be examined in more detail.
aetiologies were included, some of which contained Nevertheless, the data obtained from the current-screen-
smaller samples of patients, with the exception of the ing test for disorders of social cognition and ToM provide
CVA group. Aetiologies therefore could not be investi- a useful bedside assessment tool that should allow the cli-
gated systematically and only the effect of the side of the nician to determine the presence of ToM deficits in brain-
lesion was taken into account because of the absence of damaged patients.
prior known behavioural deficits. The aim was actually to
test different neurological populations to show that dif-
Acknowledgements
ferent pathologies could be detected as causing ToM and
social cognition deficits. However, in the second part of We thank S. Baron Cohen, A. Duchêne May-Carle, M. Monfort
the results, we analysed separately dementia, stroke pa- and I. Monfort, Ortho Editions for allowing us to use parts of their
tients and the other aetiologies, in order to show that all tests to devise our scale and the neuropsychologists who adminis-
pathologies may have social cognition impairment, but trated the GeSoCS.
the pattern varies with the aetiologies. GeSoCS sub scores
seemed also sensitive to the side of the lesions as described Disclosure Statement
in our stroke subgroup: right CVAs failed in cartoons,
inferences, ‘mind in the eyes’, and in the temporal rule The authors declare no conflict of interest.
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