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ORIGINAL ARTICLE Emotion recognition from facial expressions: a normative study of the Ekman 60-Faces Test in the Italian population Alessandra Dodich Chiara Cerami Nicola Canessa Chiara Crespi Alessandra Marcone Marta Arpone Sabrina Realmuto Stefano F. Cappa Received: 22 October 2013 / Accepted: 8 January 2014 Ó Springer-Verlag Italia 2014 Abstract The Ekman 60-Faces (EK-60F) Test is a well- known neuropsychological tool assessing emotion recogni- tion from facial expressions. It is the most employed task for research purposes in psychiatric and neurological disorders, including neurodegenerative diseases, such as the behavioral variant of Frontotemporal Dementia (bvFTD). Despite its remarkable usefulness in the social cognition research field, to date, there are still no normative data for the Italian pop- ulation, thus limiting its application in a clinical context. In this study, we report procedures and normative data for the Italian version of the test. A hundred and thirty-two healthy Italian participants aged between 20 and 79 years with at least 5 years of education were recruited on a voluntary basis. They were administered the EK-60F Test from the Ekman and Friesen series of Pictures of Facial Affect after a preliminary semantic recognition test of the six basic emo- tions (i.e., anger, fear, sadness, happiness, disgust, surprise). Data were analyzed according to the Capitani procedure [1]. The regression analysis revealed significant effects of demographic variables, with younger, more educated, female subjects showing higher scores. Normative data were then applied to a sample of 15 bvFTD patients which showed global impaired performance in the task, consistently with the clinical condition. We provided EK-60F Test normative data for the Italian population allowing the investigation of global emotion recognition ability as well as selective impairment of basic emotions recognition, both for clinical and research purposes. Keywords Social cognition Á Emotion recognition Á Ekman 60-Faces Test Á Standardization Á Behavioral variant of frontotemporal dementia Introduction Nonverbal communication is a crucial facet of social inter- action, and in its context facial expressions hold a prominent role, as defective emotion recognition can lead to ambiguous or inappropriate social interactions [2]. The ability to rec- ognize emotional facial expressions has been widely explored both in healthy subjects (see for reviews [3, 4]) and in many psychiatric and neurological condition [521]. In psychiatric disorders, affective impairments may involve the overall affective domain, as well as specific emotions processing, according to their valence. A global emotion recognition deficit, so relevant to seriously impair interpersonal relationship, is a well-known neuropsycho- logical feature of schizophrenia [5], while borderline per- sonality disorder is characterized by a prevalent impairment of negative emotional processing [6]. Fur- thermore, impairments of specific negative emotions have been reported in other psychiatric conditions, such as post- traumatic stress disorder [7] and social anxiety [8]. Specific negative emotion recognition deficits have also been reported in a variety of neurological conditions, A. Dodich (&) Á C. Cerami Á N. Canessa Á C. Crespi Á M. Arpone Á S. F. Cappa Universita ` Vita-Salute San Raffaele, Milan, Italy e-mail: [email protected] A. Dodich Á C. Cerami Á N. Canessa Á C. Crespi Á S. F. Cappa Division of Neuroscience, San Raffaele Scientific Institute, Milan, Italy C. Cerami Á A. Marcone Á S. F. Cappa Department of Clinical Neurosciences, San Raffaele Scientific Institute, Milan, Italy S. Realmuto Department of Experimental Biomedicine and Clinical Neurosciences (BioNeC), University of Palermo, Palermo, Italy 123 Neurol Sci DOI 10.1007/s10072-014-1631-x

Emotion recognition from facial expressions: a normative study of the Ekman 60-Faces Test in the Italian population

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Page 1: Emotion recognition from facial expressions: a normative study of the Ekman 60-Faces Test in the Italian population

ORIGINAL ARTICLE

Emotion recognition from facial expressions: a normative studyof the Ekman 60-Faces Test in the Italian population

Alessandra Dodich • Chiara Cerami • Nicola Canessa •

Chiara Crespi • Alessandra Marcone • Marta Arpone •

Sabrina Realmuto • Stefano F. Cappa

Received: 22 October 2013 / Accepted: 8 January 2014

� Springer-Verlag Italia 2014

Abstract The Ekman 60-Faces (EK-60F) Test is a well-

known neuropsychological tool assessing emotion recogni-

tion from facial expressions. It is the most employed task for

research purposes in psychiatric and neurological disorders,

including neurodegenerative diseases, such as the behavioral

variant of Frontotemporal Dementia (bvFTD). Despite its

remarkable usefulness in the social cognition research field,

to date, there are still no normative data for the Italian pop-

ulation, thus limiting its application in a clinical context. In

this study, we report procedures and normative data for the

Italian version of the test. A hundred and thirty-two healthy

Italian participants aged between 20 and 79 years with at

least 5 years of education were recruited on a voluntary

basis. They were administered the EK-60F Test from the

Ekman and Friesen series of Pictures of Facial Affect after a

preliminary semantic recognition test of the six basic emo-

tions (i.e., anger, fear, sadness, happiness, disgust, surprise).

Data were analyzed according to the Capitani procedure [1].

The regression analysis revealed significant effects of

demographic variables, with younger, more educated,

female subjects showing higher scores. Normative data were

then applied to a sample of 15 bvFTD patients which showed

global impaired performance in the task, consistently with

the clinical condition. We provided EK-60F Test normative

data for the Italian population allowing the investigation of

global emotion recognition ability as well as selective

impairment of basic emotions recognition, both for clinical

and research purposes.

Keywords Social cognition � Emotion recognition �Ekman 60-Faces Test � Standardization � Behavioral

variant of frontotemporal dementia

Introduction

Nonverbal communication is a crucial facet of social inter-

action, and in its context facial expressions hold a prominent

role, as defective emotion recognition can lead to ambiguous

or inappropriate social interactions [2]. The ability to rec-

ognize emotional facial expressions has been widely

explored both in healthy subjects (see for reviews [3, 4]) and

in many psychiatric and neurological condition [5–21].

In psychiatric disorders, affective impairments may

involve the overall affective domain, as well as specific

emotions processing, according to their valence. A global

emotion recognition deficit, so relevant to seriously impair

interpersonal relationship, is a well-known neuropsycho-

logical feature of schizophrenia [5], while borderline per-

sonality disorder is characterized by a prevalent

impairment of negative emotional processing [6]. Fur-

thermore, impairments of specific negative emotions have

been reported in other psychiatric conditions, such as post-

traumatic stress disorder [7] and social anxiety [8].

Specific negative emotion recognition deficits have also

been reported in a variety of neurological conditions,

A. Dodich (&) � C. Cerami � N. Canessa � C. Crespi �M. Arpone � S. F. Cappa

Universita Vita-Salute San Raffaele, Milan, Italy

e-mail: [email protected]

A. Dodich � C. Cerami � N. Canessa � C. Crespi � S. F. Cappa

Division of Neuroscience, San Raffaele Scientific Institute,

Milan, Italy

C. Cerami � A. Marcone � S. F. Cappa

Department of Clinical Neurosciences, San Raffaele Scientific

Institute, Milan, Italy

S. Realmuto

Department of Experimental Biomedicine and Clinical

Neurosciences (BioNeC), University of Palermo, Palermo, Italy

123

Neurol Sci

DOI 10.1007/s10072-014-1631-x

Page 2: Emotion recognition from facial expressions: a normative study of the Ekman 60-Faces Test in the Italian population

ranging from focal brain lesions to neurodegenerative

disorders. These include traumatic brain injuries [9, 10],

temporal lobe epilepsy [11], Parkinson’s disease [12], and

amyotrophic lateral sclerosis [13]. Patients affected by

Alzheimer’s dementia are mostly characterized by an

overall emotion recognition impairment irrespective of the

stimuli affective valence [14] and similar findings have

been reported in the behavioral variant of frontotemporal

dementia (bvFTD) [15–18]. In the context of the fronto-

temporal lobar degeneration spectrum of disorders, other

clinical subtypes, as progressive supranuclear palsy [19]

and primary progressive aphasia [20, 21] may present

emotion recognition impairments, even though these are

not core features of the clinical presentation.

The Ekman 60-Faces (EK-60F) Test [22] is a well-

known task which allows both to investigate overall emo-

tion recognition performance and to identify basic emotion

(i.e., fear, disgust, anger, happiness, sadness, surprise)

recognition impairments, providing a comprehensive

assessment of this facet of social cognition.

Notwithstanding the remarkable usefulness of the EK-

60F Test, to date, there are still no normative data for the

Italian population, thus limiting its clinical use. Therefore,

the aim of this study is to supply standardization and

normative data for the Italian version of the EK-60F Test to

provide a valid neuropsychological tool for the identifica-

tion of emotion recognition deficits. In addition, we tested

the EK-60F Test performance of 15 bvFTD patients as an

example of its clinical application in a disorder typically

characterized by prominent social cognition impairments.

Methods

Participants

A sample of 132 healthy Italian adults [67 women: mean

age = 51.11 years, standard deviation (SD) = 16.50;

mean education = 12.62 years, SD = 4.40; 65 men: mean

age = 48.62 years, SD = 16.16; mean education =

13.90 years, SD = 4.41] were recruited on voluntary basis

for the normative procedure (Table 1). Inclusion criteria

were no history or clinical evidence of neurological or

psychiatric diseases, and a Mini Mental State Examination

(MMSE) raw score C28 in subjects with education

C8 years or C27 in subjects with education B8 years

(mean = 29.22; SD = 0.79).

A group of 15 mild-dementia patients fulfilling clinical

consensus criteria for probable bvFTD [23, 24] (Table 2)

were consecutively recruited from the Department of Clin-

ical Neurosciences, San Raffaele Scientific Institute (Milan,

Italy), and evaluated by a team of experienced behavioral

neurologists and neuropsychologists. Exclusion criteria for

the recruitment of bvFTD patients were: MMSE raw score

\21 (mean = 24.53; SD = 1.99), Clinical Dementia Rat-

ing Scale (CDR) global score [1 (CDR sum of boxes

mean = 4.54; SD = 1.63), and a positive history of other

neuropsychiatric disorders or evidence of other pathologies

on MRI scan. All subjects, both healthy controls and patients,

gave informed consent to the experimental procedure that

had been approved by the local Ethical Committee.

Task procedure

Subjects were administered the EK-60F Test after a pre-

liminary semantic recognition test of the basic emotions, in

which they were asked to verbally provide an example for

each of the six emotions (e.g., ‘‘Give me an example of a

situation in which you feel happy’’ ‘‘I am happy when I

receive a gift’’). Any incorrect answer led to the exclusion

from the present study (no subject was excluded).

The EK-60F Test consists of 60 b/w pictures from the

Ekman and Friesen series of Picture of Facial Affect [22],

which depict the faces of 10 actors (6 female, 4 male), each

displaying six basic emotions (i.e., happiness, sadness,

anger, fear, surprise, disgust). A global score (GS) of 60

indicates the best possible performance and each basic

emotion has a sub-score of a maximum of 10 points. The

Italian version of the test was created using as reference the

computer software available on CD-ROM for the American

version. Each image presented the face of an actor and

below it the labels of the Italian words for the six

Table 1 Demographic data of the 132 healthy controls

Education in years Age in years

20–29 30–39 40–49 50–59 60–69 70–79 Total (F/M) Total

3–8 1/0 0/0 3/3 4/4 7/6 5/1 20/14 34

9–13 1/5 2/2 4/2 7/7 4/3 4/1 22/20 42

[13 6/8 4/5 2/3 6/6 3/7 4/2 25/31 56

Total (F/M) 8/13 6/7 9/8 17/17 14/16 13/4 67/65 132

Total 21 13 17 34 30 17 132 –

In each cell, the number of participants as females/males is reported

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investigated emotions. Subjects were required to answer

verbally choosing the label that best described the facial

expression shown by the actor. Images were shown each

for 5 s, according to the Ekman and Friesen procedure

[22]. Six trial runs preceded the real EK-60F Test, con-

sisting of an example of each emotion performed by an

actor who did not appear in the test phase.

Statistical methods

Descriptive statistics were estimated for GS and each

emotion sub-score. For GS, seven different linear regres-

sion analyses were performed, to establish which demo-

graphic variables, enclosing gender, age and years of

education (including their quadratic, logarithmic and

square-root terms), had to be included in the final model, as

the most effective in reducing the residual variance.

Adjusted values were calculated by adding (or sub-

tracting) the contribution of each variable for each subject

[1]. Correction grid was then derived to adjust the perfor-

mance of each newly tested individual for the effect of the

demographic variables. Finally, we classified the adjusted

GS into five categories (from 0 to 4) [1], namely the

equivalent scores (ES). The ‘‘0’’ score corresponds to each

score located below the outer unidirectional non-paramet-

ric tolerance limit, with a confidence of 95 % (the third

observation for 132 subjects [25]). The ‘‘4’’ score corre-

sponds to the median and above median values, and the

‘‘1’’, ‘‘2’’, and ‘‘3’’ are intermediate values on a quasi-

interval scale calculated with reference to the left half of

the distribution [1].

To analyze the effect of demographic variables on the

recognition performance for each emotion, correlation

analyses were computed between age and education and

single emotion sub-scores. Moreover, the effect of gender

on each emotion was determined contrasting the perfor-

mance of males and females. Both analyses failed in

revealing an overall effect of demographic variables on

single emotions sub-scores and as a consequence, only a

cut-off value was established for each emotion to separate

normal from pathological performances.

For each emotion, the observations were ranked

according to an increasing ordinal scale and the cut-off was

established according to the lowest tolerance limit, esti-

mating the score corresponding to the fifth centile of the

population. The choice of using non-parametric limits was

due to the non-normal shape of each emotion sub-scores

distribution.

Statistical analyses were performed with STATISTICA

8 software (http://www.statsoft.com).

Results

Normative data

The descriptive scores for GS and single emotion sub-scores

are reported in Table 3. The final model of multiple

regression for GS showed age, education in years and gender

as the best predictors of the GS performance

[F(3,128) = 13.92, p \ 0.0001], with higher scores for

younger, more educated and female subjects. Table 4 reports

Table 2 BvFTD demographic data and Ekman 60-Faces (EK-60F) Test global scores (GS) with relative equivalent scores (ES)

Patient Demographic data Ek-60F scores

Age Education Gender GS raw score GS adjusted score GS ES Emotions under cut-off

1 52 10 M 34 36.02 0 A

2 71 12 M 31 34.84 0 H/F

3 71 7 M 27 32.83 0 S/H/D/Sa

4 67 13 F 17 19.50 0 S/H/A/Sa

5 59 17 M 28 28.34 0 S/A

6 64 13 M 29 31.88 0 A/Sa

7 78 8 F 31 38.35 1 S/H/A

8 73 17 M 22 25.20 0 S/F/D/A

9 52 5 M 22 25.21 0 S/H/D/A

10 71 17 M 23 25.24 0 S/H/F/A/Sa

11 71 8 M 24 29.83 0 S/A/Sa

12 62 8 M 23 26.92 0 F/D/Sa

13 65 11 F 31 33.5 0 H/D

14 41 13 M 15 13.12 0 S/H/F/D/A/Sa

15 65 5 M 19 25.07 0 S/H/D/A/Sa

On the last column emotions sub-scores (i.e., S surprise; H happiness; F fear; D disgust; A anger; Sa sadness) under cut-off are reported

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the correction factors to be added or subtracted from raw GS.

Consistently with the original normative data [22], the

analyses on single emotions sub-scores highlighted higher

means (and cut-off scores) for positive emotions (happiness

cut-off = 9, surprise cut-off = 6) and lower means for

negative facial expressions, with fear obtaining the lowest

cut-off (=2). Single emotion cut-off scores are reported in

Table 5 together with the ES for the global score.

Emotion recognition assessment in the bvFTD sample

We applied the normative procedure to a sample of 15

bvFTD patients to test its use in clinical practice. As

expected, the majority of the bvFTD patients (14/15) had

an impaired overall performance (GS ES = 0) and only

one subject showed a borderline performance (GS

ES = 1). Single basic emotions were heterogeneously

recognized among subjects (Table 2): in particular, 12

bvFTD patients showed impaired recognition of both

negative and positive emotions, while three patients had a

selective deficit of negative affective states (i.e., subjects

#1, #6 and #12). No differences were found between these

two groups of patients for demographic (i.e., age and

education), clinical variables (i.e., CDR sum of boxes) and

MMSE score.

In the bvFTD sample, anger was the most misrecognized

emotion (i.e., 11/15 patients) followed by surprise, happi-

ness, sadness, disgust and lastly fear, which was not rec-

ognized by only five patients.

Discussion

In this study, we provided standardization and normative

data for the Italian version of the EK-60F Test analyzing

the performances of a large sample of 132 Italian healthy

individuals with respect to the main socio-demographic

variables (i.e., age, gender and education).

The EK-60F GS descriptive and normative data for the

Italian population obtained by our sample of healthy sub-

jects are comparable with those obtained in American

Table 3 Raw descriptive values of the Ekman 60-Faces (EK-60F)

Test global score and single emotions sub-scores in 132 healthy

subjects

Mean SD Median Min Max 95 %

Confidence

interval

Global score 49.40 5.23 50 33 58 48.50–50.3

Surprise 9.04 1.27 9 4 10 8.81–9.26

Happiness 9.80 0.52 10 7 10 9.71–9.89

Fear 6.24 2.62 6 0 10 5.79–6.69

Disgust 8.47 1.64 9 2 10 8.18–8.75

Anger 7.85 1.61 8 3 10 7.57–8.12

Sadness 8.01 1.82 8 0 10 7.69–8.32

Table 4 Age, gender and education adjustment grid for the Ekman 60-Faces (EK-60F) Test global score (GS)

Education Age

20 25 30 35 40 45 50 55 60 65 70 75 80

5 $ -2.89 -1.93 -0.98 -0.03 0.93 1.88 2.83 3.78 4.74 5.69 6.64 7.60 8.55

# -2.50 -1.55 -0.60 0.36 1.30 2.26 3.21 4.17 5.12 6.07 7.03 7.98 8.93

8 $ -4.08 -3.13 -2.18 -1.22 -0.27 0.68 1.64 2.59 3.54 4.49 5.45 6.40 7.35

# -3.70 -2.75 -1.79 -0.84 0.11 1.07 2.02 2.97 3.92 4.88 5.83 6.78 7.73

13 $ -6.08 -5.12 -4.17 -3.22 -2.26 -1.31 -0.36 0.60 1.55 2.50 3.45 4.41 5.36

# -5.69 -4.74 -3.79 -2.83 -1.88 -0.93 0.03 0.98 1.93 2.88 3.84 4.79 5.74

17 $ -7.67 -6.72 -5.76 -4.81 -3.86 -2.90 -1.95 -1 -0.05 0.90 1.86 2.81 3.77

# -7.29 -6.33 -5.38 -4.43 -3.47 -2.52 -1.57 -0.62 0.34 1.29 2.24 3.20 4.15

Corrected EK-60F GS female = raw score ? 0.190 9 (age - 51.41) - 0.40 9 (education - 13.26) - 0.19

Corrected EK-60F GS male = raw score ? 0.190 9 (age - 51.41) - 0.40 9 (education - 13.26) ? 0.19

Table 5 Equivalent scores (ES), intervals for global score (GS) and cut-off scores for single emotions

Equivalent score GS Surprise Happiness Fear Disgust Anger Sadness

0 0–37.46 \6 \9 \2 \4 \5 \4

1 37.47–41.62 – – – – – –

2 41.63–45.79 – – – – – –

3 45.80–49.95 – – – – – –

4 49.96–60 – – – – – –

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subjects [22]. The EK-60F GS distribution was correlated

with gender, age and years of education, resulting in a

better performance for female, younger and more educated

subjects. This result is consistent with previous studies

showing an advantage in emotion recognition for female

healthy subjects [26],which has been partially ascribed to

differences in specific patterns of neural responses to

emotional faces [26, 27]. On the other hand, a large liter-

ature (e.g., [28, 29]) reported an increased difficulty for

older adults in recognizing some basic emotions, possibly

due to age-related changes in the volume of ‘‘social brain’’

[30], mainly involving frontal and temporal lobe [29],

rather than to a decline of basic perceptual skills. In fact,

notwithstanding the effect of aging on basic perceptual

factors [31], previous literature provided evidence of the

independence of emotion recognition decline from basic

face processing deterioration [28].

On the other hand, to our knowledge the relationship

between education and emotion recognition ability was not

specifically investigated in previous studies. In this study,

we provided evidence of an increasing EK-60F global

performance according to the educational level of the

subjects. This result is consistent with previous normative

works [32] supporting the general role of education in

predicting cognitive performance in multiple neuropsy-

chological tests.

Exploring the distribution of the six emotion sub-

scores, we did not find any significant effect of the

demographic variables on subjects’ performances. This

finding is broadly in line with previous studies, which

failed to prove a common effect of demographic variables

on different facial expressions processing [27–29]. The

assessment of specific emotions confirmed previous liter-

ature data [10, 22], according to which happiness was the

easiest emotion to be recognized by healthy subjects,

followed by surprise.

In contrast, control subjects experienced significantly

more difficulties in judging negative facial emotions of

anger, sadness, disgust, and fear. Among negative emo-

tions, fear was the most difficult to recognize, contrary to

anger, in which healthy subjects obtained the highest

scores. These results confirm previous findings on healthy

subjects [10, 15], proving anger and fear as an ‘‘easy’’ and

‘‘difficult’’ emotion to identify, respectively. The results for

single emotions in our healthy sample mirror this distinc-

tion between positive and ‘‘easy/difficult’’ negative emo-

tions, with higher cut-off scores for positive affective states

(happiness = 9 and surprise = 6) and lower cut-off scores

for negative emotions, of which anger and fear represent

the opposite extremes. The usefulness of this clinical tool

has been demonstrated by applying correction grid, ES and

single emotion cut-off scores to the performances of 15

mild bvFTD patients. Overall, patients presented a deficit

in facial expression recognition, accompanied by variable

impairments of single emotions. Eighty percent of the

bvFTD sample showed both negative and positive emotion

recognition deficits, consistently with previous studies

showing a facial expression processing deficit in bvFTD

irrespective of the affective valence of the stimulus [17,

18]. Twenty percent of the patient sample, however,

showed a selective impairment in processing stimuli with

negative affective valence. Given that demographic vari-

ables and clinical indexes in these patients did not differ

from those of the rest of the sample, a prevalent involve-

ment of temporal regions, whose damage is selectively

associated with an impairment of negative emotions rec-

ognition [17], can be hypothesized in these patients. In the

absence of imaging correlations, however, this remains a

speculation.

Analyses of single emotions sub-scores identified anger

as the most difficult emotion to be recognized by bvFTD

patients, while fear was frequently preserved. These results

possibly reflect specific effects of the recognition of these

two emotions in the normative population. In conclusion,

our data on bvFTD patients not only confirm previous

studies that highlight an overall emotion recognition

impairment, but also stress the utility of the EK-60F Test in

detecting a specific affective processing deficit in mild-

dementia patients. Moreover, we proved in bvFTD patients

a deficit in both ‘‘easy’’ and ‘‘difficult’’ negative emotions

recognition, supporting a specific impairment of facial

expression processing not closely related to a general

cognitive decline (see also [15]).

In conclusion, the EK-60F Test normative data for the

Italian population may prove useful for both clinical and

research purposes to investigate global emotion recognition

ability as well as putative selective impairment of basic

emotions recognition. As a note of caution, despite the

good concordance between single emotions cut-off and

normative scores previously reported [22], considering the

effects of non-parametric statistics on the cut-off compu-

tation, a more thorough investigation of specific emotion

deficits is advisable in patients who show borderline scores,

particularly in the case of fear.

Emotion recognition impairments are reported in neu-

rodegenerative disorders, such as bvFTD, as well as in

many other neuropsychiatric conditions as main or

accompanying symptoms which crucially affect patient’s

social skills and behavior. The assessment of emotion

recognition ability might be indeed important not only for

the characterization of patient’s neuropsychological profile

but also for management evaluations on disease progres-

sion and caregiver burden.

Finally, the interpretation of the EK-60F performance

may not be irrespective of the overall and specific cognitive

functioning, as poor performances on the EK-60F Test

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might be due to the presence of deficits in other cognitive

domains (e.g., executive and sematic processing).

Acknowledgments We thank Francesca Cortese, Leonardo Iacca-

rino and Federica Biotti for their help in the collection of neuropsy-

chological data and Eleonora Catricala and Pasquale Anthony Della

Rosa for the statistical support.

References

1. Capitani E, Laiacona M (1997) Composite neuropsychological

batteries and demographic correction: standardization based on

equivalent scores, with a review of published data. The Italian

Group for the Neuropsychological Study of Ageing. J Clin Exp

Neuropsychol 19(6):795–809. doi:10.1080/01688639708403761

2. Adolphs R (2003) Cognitive neuroscience of human social

behaviour. Nat Rev Neurosci 4(3):165–178. doi:10.1038/

nrn1056nrn1056

3. Phan KL, Wager T, Taylor SF, Liberzon I (2002) Functional

neuroanatomy of emotion: a meta-analysis of emotion activation

studies in PET and fMRI. Neuroimage 16(2):331–348. doi:10.

1006/nimg.2002.1087S1053811902910876

4. Fusar-Poli P, Placentino A, Carletti F, Landi P, Allen P, Surg-

uladze S, Benedetti F, Abbamonte M, Gasparotti R, Barale F,

Perez J, McGuire P, Politi P (2009) Functional atlas of emotional

faces processing: a voxel-based meta-analysis of 105 functional

magnetic resonance imaging studies. J Psychiatry Neurosci

34(6):418–432

5. Kohler CG, Walker JB, Martin EA, Healey KM, Moberg PJ

(2010) Facial emotion perception in schizophrenia: a meta-ana-

lytic review. Schizophr Bull 36(5):1009–1019. doi:10.1093/

schbul/sbn192sbn192

6. Unoka Z, Fogd D, Fuzy M, Csukly G (2011) Misreading the

facial signs: specific impairments and error patterns in recogni-

tion of facial emotions with negative valence in borderline per-

sonality disorder. Psychiatry Res 189(3):419–425. doi:10.1016/j.

psychres.2011.02.010S0165-1781(11)00102-8

7. Poljac E, Montagne B, de Haan EH (2011) Reduced recognition

of fear and sadness in post-traumatic stress disorder. Cortex

47(8):974–980. doi:10.1016/j.cortex.2010.10.002S0010-9452(10)

00243-1

8. Montagne B, Schutters S, Westenberg HG, van Honk J, Kessels

RP, de Haan EH (2006) Reduced sensitivity in the recognition of

anger and disgust in social anxiety disorder. Cogn Neuropsychi-

atry 11(4):389–401. doi:76990331110.1080/13546800444000254

9. Croker V, McDonald S (2005) Recognition of emotion from

facial expression following traumatic brain injury. Brain Inj

19(10):787–799

10. Rapcsak SZ, Galper SR, Comer JF, Reminger SL, Nielsen L,

Kaszniak AW, Verfaellie M, Laguna JF, Labiner DM, Cohen RA

(2000) Fear recognition deficits after focal brain damage: a

cautionary note. Neurology 54(3):575–581

11. Meletti S, Benuzzi F, Cantalupo G, Rubboli G, Tassinari CA,

Nichelli P (2009) Facial emotion recognition impairment in

chronic temporal lobe epilepsy. Epilepsia 50(6):1547–1559.

doi:10.1111/j.1528-1167.2008.01978.xEPI1978

12. Ariatti A, Benuzzi F, Nichelli P (2008) Recognition of emotions

from visual and prosodic cues in Parkinson’s disease. Neurol Sci

29(4):219–227. doi:10.1007/s10072-008-0971-9

13. Zimmerman EK, Eslinger PJ, Simmons Z, Barrett AM (2007)

Emotional perception deficits in amyotrophic lateral sclerosis.

Cogn Behav Neurol 20(2):79–82. doi:10.1097/WNN.

0b013e31804c700b00146965-200706000-00001

14. Bediou B, Ryff I, Mercier B, Milliery M, Henaff MA, D’Amato

T, Bonnefoy M, Vighetto A, Krolak-Salmon P (2009) Impaired

social cognition in mild Alzheimer disease. J Geriatr Psychiatry

Neurol 22(2):130–140. doi:10.1177/08919887093329390891988

709332939

15. Fernandez-Duque D, Black SE (2005) Impaired recognition of

negative facial emotions in patients with frontotemporal demen-

tia. Neuropsychologia 43(11):1673–1687. doi:S0028-3932(05)

00057-610.1016/j.neuropsychologia.2005.01.005

16. Lough S, Kipps CM, Treise C, Watson P, Blair JR, Hodges JR

(2006) Social reasoning, emotion and empathy in frontotemporal

dementia. Neuropsychologia 44(6):950–958. doi:S0028-3932(05)

00277-010.1016/j.neuropsychologia.2005.08.009

17. Rosen HJ, Pace-Savitsky K, Perry RJ, Kramer JH, Miller BL,

Levenson RW (2004) Recognition of emotion in the frontal and

temporal variants of frontotemporal dementia. Dement Geriatr

Cogn Disord 17(4):277–281. doi:10.1159/00007715477154

18. Diehl-Schmid J, Pohl C, Ruprecht C, Wagenpfeil S, Foerstl H,

Kurz A (2007) The Ekman 60 Faces Test as a diagnostic

instrument in frontotemporal dementia. Arch Clin Neuropsychol

22(4):459–464. doi:S0887-6177(07)00041-810.1016/j.acn.2007.

01.024

19. Ghosh BC, Rowe JB, Calder AJ, Hodges JR, Bak TH (2009)

Emotion recognition in progressive supranuclear palsy. J Neurol

Neurosurg Psychiatry 80(10):1143–1145. doi:10.1136/jnnp.2008.

15584680/10/1143

20. Rohrer JD, Sauter D, Scott S, Rossor MN, Warren JD (2012)

Receptive prosody in nonfluent primary progressive aphasias.

Cortex 48(3):308–316. doi:10.1016/j.cortex.2010.09.004S0010-

9452(10)00238-8

21. Calabria M, Cotelli M, Adenzato M, Zanetti O, Miniussi C (2009)

Empathy and emotion recognition in semantic dementia: a case

report. Brain Cogn 70(3):247–252. doi:10.1016/j.bandc.2009.02.

009S0278-2626(09)00038-4

22. Ekman P, Friesen W (1976) Pictures of facial affect. Consulting

Psychologists Press, Palo Alto

23. Rascovsky K, Hodges JR, Knopman D, Mendez MF, Kramer JH,

Neuhaus J, van Swieten JC, Seelaar H, Dopper EG, Onyike CU,

Hillis AE, Josephs KA, Boeve BF, Kertesz A, Seeley WW,

Rankin KP, Johnson JK, Gorno-Tempini ML, Rosen H, Prioleau-

Latham CE, Lee A, Kipps CM, Lillo P, Piguet O, Rohrer JD,

Rossor MN, Warren JD, Fox NC, Galasko D, Salmon DP, Black

SE, Mesulam M, Weintraub S, Dickerson BC, Diehl-Schmid J,

Pasquier F, Deramecourt V, Lebert F, Pijnenburg Y, Chow TW,

Manes F, Grafman J, Cappa SF, Freedman M, Grossman M,

Miller BL (2011) Sensitivity of revised diagnostic criteria for the

behavioural variant of frontotemporal dementia. Brain 134(Pt

9):2456–2477. doi:10.1093/brain/awr179awr179

24. Neary D, Snowden JS, Gustafson L, Passant U, Stuss D, Black S,Freedman M, Kertesz A, Robert PH, Albert M, Boone K, Miller

BL, Cummings J, Benson DF (1998) Frontotemporal lobar

degeneration: a consensus on clinical diagnostic criteria. Neu-

rology 51(6):1546–1554

25. Wilks SS (1941) Determination of sample sizes for setting tol-

erance limits. Ann Math Stat 12:91–96

26. McClure EB (2000) A meta-analytic review of sex differences in

facial expression processing and their development in infants,

children, and adolescents. Psychol Bull 126(3):424–453

27. Lee TM, Liu HL, Hoosain R, Liao WT, Wu CT, Yuen KS, Chan

CC, Fox PT, Gao JH (2002) Gender differences in neural cor-

relates of recognition of happy and sad faces in humans assessed

by functional magnetic resonance imaging. Neurosci Lett

333(1):13–16. doi:S0304394002009655

28. Sullivan S, Ruffman T (2004) Emotion recognition deficits in the

elderly. Int J Neurosci 114(3):403–432. doi:10.1080/002074

50490270901H6YBRR4W08PXACL8

Neurol Sci

123

Page 7: Emotion recognition from facial expressions: a normative study of the Ekman 60-Faces Test in the Italian population

29. Ruffman T, Henry JD, Livingstone V, Phillips LH (2008) A

meta-analytic review of emotion recognition and aging: impli-

cations for neuropsychological models of aging. Neurosci Bio-

behav Rev 32(4):863–881. doi:10.1016/j.neubiorev.2008.01.

001S0149-7634(08)00010-9

30. Brothers L (1990) The social brain: a project for integrating

primate behaviour and neurophysiology in a new domain. Con-

cepts Neurosci 1:27–51

31. Hedden T, Gabrieli JDE (2004) Insights into the ageing mind: a

view from cognitive neuroscience. Nat Rev Neurosci 5(2):87–96.

doi:10.1038/Nrn1323

32. Bianchi A, Pra MD (2008) Twenty years after Spinnler and Tog-

noni: new instruments in the Italian neuropsychologist’s toolbox.

Neurolo Sci 29(4):209–217. doi:10.1007/s10072-008-0970-x

Neurol Sci

123